European Journal of Phycology

ISSN: 0967-0262 (Print) 1469-4433 (Online) Journal homepage: https://www.tandfonline.com/loi/tejp20

Dissolved organic matter (DOM) release by

phytoplankton in the contemporary and future
ocean

Daniel C.O. Thornton

To cite this article: Daniel C.O. Thornton (2014) Dissolved organic matter (DOM) release by
phytoplankton in the contemporary and future ocean, European Journal of Phycology, 49:1,
20-46, DOI: 10.1080/09670262.2013.875596

To link to this article: https://doi.org/10.1080/09670262.2013.875596

Published online: 12 Feb 2014.

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 Eur. J. Phycol. (2014), 49(1): 20–46

Dissolved organic matter (DOM) release by phytoplankton in

the contemporary and future ocean

DANIEL C.O. THORNTON

Department of Oceanography, Eller O & M Building, Texas A & M University, College Station, TX 77843-3146, U.S.A.

(Received 30 March 2013; revised 3 September 2013; accepted 3 September 2013)

The partitioning of organic matter (OM) between dissolved and particulate phases is an important factor in determining the fate of
organic carbon in the ocean. Dissolved organic matter (DOM) release by phytoplankton is a ubiquitous process, resulting in
2–50% of the carbon fixed by photosynthesis leaving the cell. This loss can be divided into two components: passive leakage by
diffusion across the cell membrane and the active exudation of DOM into the surrounding environment. At present there is no
method to distinguish whether DOM is released via leakage or exudation. Most explanations for exudation remain hypothetical; as
while DOM release has been measured extensively, there has been relatively little work to determine why DOM is released.
Further research is needed to determine the composition of the DOM released by phytoplankton and to link composition to
phytoplankton physiological status and environmental conditions. For example, the causes and physiology of phytoplankton cell
death are poorly understood, though cell death increases membrane permeability and presumably DOM release. Recent work has
shown that phytoplankton interactions with bacteria are important in determining both the amount and composition of the DOM
released. In response to increasing CO2 in the atmosphere, climate change is creating increasingly stressful conditions for
phytoplankton in the surface ocean, including relatively warm water, low pH, low nutrient supply and high light. As ocean physics
and chemistry change, it is hypothesized that a greater proportion of primary production will be released directly by phytoplankton
into the water as DOM. Changes in the partitioning of primary production between the dissolved and particulate phases will have
bottom-up effects on ecosystem structure and function. There is a need for research to determine how these changes affect the fate
of organic matter in the ocean, particularly the efficiency of the biological carbon pump.

Key words: autocatalytic cell death, carbon cycle, cell permeability, climate change, DOC, exopolymer, exudation, global
warming, microbial foodwebs, ocean acidification, PER, phytoplankton physiology, programmed cell death, TEP, transparent
exopolymer particles

Introduction matter (DOM) rather than particulate organic matter

The ocean covers 71% of the Earth’s surface, with
photosynthesis in sunlit surface waters directly or
indirectly supporting the majority of food webs in
marine ecosystems. Based on satellite observations,
net primary productivity of the global ocean is esti-
mated to be 45–55 Pg C yr−1 (1 Pg = 1 Gt = 1015 g)
(Longhurst et al., 1995; Field et al., 1998; Falkowski
et al., 2000; Carr et al., 2006; Westberry et al., 2008).
This estimate is 40–50% of the primary productivity
of the total biosphere. There is an estimated 1–2 Pg C
associated with living organisms in the ocean
(Falkowski et al., 2000), of which between 0.25 and
0.65 Pg C are phytoplankton (Falkowski & Raven,
2007).The pool of non-living organic carbon in the
ocean is estimated to be much greater than the living
component at 1000 Pg C (Falkowski & Raven, 2007)
and most of this is in the form of dissolved organic
Correspondence to Daniel Thornton. E-mail: dthornton@ocean.
tamu.edu
ISSN 0967-0262 (print)/ISSN 1469-4433 (online)/14/010020-46 © 2014 British Phycological Society
http://dx.doi.org/10.1080/09670262.2013.875596
(POM). Hansell et al. (2009) estimated that the oceans
contain 662 Pg C as dissolved organic carbon (DOC),
which is within the range of the amount of carbon in
CO2 in the atmosphere over recent history (612 Pg C
in 1850 and 784 Pg C in 2000: Emerson & Hedges,
2008). The division between dissolved and particulate
organic matter is operationally defined by the pore
size used by researchers to separate the two fractions.
Marine chemists generally use GF/F filters (Whatman,
Maidstone, U.K.), as these glass fibre filters may be
combusted to remove organic contamination (Wurl &
Sin, 2009). The average pore size of a GF/F filter is 0.7
µm, which is significantly larger than many abundant
particles in the ocean; viruses, for example, are gen-
erally 0.1 µm in diameter and found at concentrations
of 109 to 1011 L−1 (Suttle, 2005). Despite the limita-
tions of an operational definition, marine DOM is
nonetheless a major reservoir of carbon, and under-
standing the factors affecting the production, loss and
turnover of DOM are essential to understand the

Published online 12 Feb 2014

Phytoplankton DOM release
dynamics of the global carbon cycle. DOM is the
major carbon source for heterotrophic prokaryotes in
the water column. Some DOM binds trace elements in
the ocean and this is particularly important in the case
of iron, which limits phytoplankton growth in a sig-
nificant proportion of the open ocean (Emerson &
Hedges 2008). DOM also attenuates UV radiation in
the surface ocean and serves as a catalyst for photo-
chemical reactions (Emerson & Hedges, 2008). The
partitioning of organic carbon between the dissolved
and particulate pools has implications for the export of
organic matter from the photic zone and its ultimate
fate, as while particulate organic carbon (POC) sinks,
DOC does not (Borchard & Engel, 2012).
A number of processes cause the contents of phy-
toplankton cells to be released into surrounding sea-
water as DOM. These processes include sloppy
feeding by predators (Møller et al., 2003; Møller,
2007), lytic viral infections (Bratbak et al., 1993;
Gobler et al., 1997, Bettarel et al., 2005), and cell
death (Veldhuis et al., 2001). Moreover, living phyto-
plankton cells exude a significant proportion, and
under some circumstances the majority, of their photo-
synthate into the surrounding medium (Fogg, 1983;
Wood & Van Valen, 1990). There are major gaps in
our understanding of the physiology and biogeochem-
ical significance of DOM release by phytoplankton
(Flynn et al., 2008).
The objective of this review is to synthesize what
is currently known about DOM release by phyto-
plankton, building on previous reviews (Hellebust,
1974; Fogg, 1983; Williams, 1990; Myklestad, 2000;
Nagata, 2000). I will focus on the physiological
processes that affect DOM production by the phyto-
plankton themselves, rather than physical disruption
processes (i.e. sloppy feeding and viral lysis). Within
this framework I will emphasize the interaction
between phytoplankton DOM production and global
climate change. The increase in CO2 in the atmo-
sphere as a result of human activity (IPCC, 2013) is
causing the ocean to become both warmer (Levitus
et al., 2000) and more acidic (Caldeira & Wickett,
2003; Royal Society, 2005) and there is an urgent
need to understand how ecosystems and global bio-
geochemical cycles will respond. In this review I will
bring together what little we know about the effects
of ocean temperature and pH on DOM release by
phytoplankton and suggest future research
directions.
Production rates of DOM by phytoplankton
DOM release by phytoplankton has been measured in
laboratory culture for specific organisms under highly
controlled conditions, and in natural populations in
the field, and it has been constrained in ecosystem
models. Production rates of DOM by phytoplankton
are usually expressed as Percentage Extracellular
21
Release (PER). Total primary production (TPP) can
be divided into particulate primary production (PPP)
and dissolved primary production (DPP). PER is sim-
ply DPP/TPP × 100 (Marañón et al., 2005; Morán
et al., 2006). While PER is a useful parameter to
understand the physiology of phytoplankton, it is not
as useful as the absolute measures of carbon flux for
understanding the biogeochemistry of ecosystems.
For example, in situations where PER is relatively
constant, the amount of carbon exuded into the envir-
onment as DOM may be highly variable because
primary productivity varies in response to environ-
mental factors such as light availability. For this rea-
son, some researchers have argued that the concept of
PER should be abandoned (Smith & Wiebe, 1976;
Mague et al., 1980).
DPP and PPP have been measured by essentially
the same method over the last 50 years, which is an
extension of Steemann-Nielsen’s (1952) revolution-
ary method for measuring primary productivity using
14
C as a tracer. Samples of culture or natural waters are
incubated in a bottle with a radioactive inorganic
carbon source (NaH14CO3). During photosynthesis
the radioactive inorganic carbon is fixed into organic
carbon, which may be incorporated into the cell as
PPP, exuded into the surrounding medium as DPP, or
respired back to inorganic carbon. At the end of the
timed incubation, PPP is separated from DPP by fil-
tration. Unassimilated radioactive inorganic carbon is
driven off the samples by acidification and the amount
of radioactive carbon incorporated into the DPP and
PPP is counted and used to calculate PER (Hellebust,
1965; Morán et al., 2006). Sources of error in this
technique include the transformation of PPP to DPP
through cell lysis during filtration (Sharp, 1977) and
the binding of DOM to the filters (Karl et al., 1998;
Morán et al., 1999).
High temperature catalytic oxidation (HTCO)
instruments for the measurement of dissolved organic
carbon (DOC) were developed in the late 1980s
(Sugimura & Suzuki, 1988). The interpretation of
the data produced from this method remained contro-
versial for a number of years as it was often unclear
what was being measured, mainly due to issues asso-
ciated with preparing DOM-free water for blanks and
the lack of standardized reference water samples for
inter-laboratory comparisons (Hedges et al., 1993;
Benner & Strom, 1993; Suzuki, 1993). However,
these issues were resolved and the HTCO technique
enabled DOM release by phytoplankton to be deter-
mined by simply measuring how much of the total
organic carbon was allocated to the dissolved and
particulate fractions over time, either in phytoplank-
ton cultures (Chen & Wangersky, 1996; Biddanda &
Benner, 1997) or in incubations of natural waters
(Wetz & Wheeler, 2003). An advantage of this tech-
nique is that it avoids the safety issues and permissions
involved with handling radioisotopes. Dissolved and
D. C. O. Thornton
particulate organic carbon are usually separated by
filtration and are therefore prone to the same filtration
artefacts as 14C tracer methods.
PER in phytoplankton cultures
Hellebust (1965) made the first extensive measure-
ments of PER by 22 species in laboratory grown
cultures and concluded that phytoplankton release
3–6% of their photoassimilated carbon during expo-
nential growth. Nagata (2000) summarized PER mea-
surements from laboratory experiments with 37
species, including the work of Hellebust (1965).
Nagata concluded that mean PER in cultures is 5%
(range 2–10%), with higher rates in stressed cultures
(nutrient limitation or suboptimal conditions of light
and temperature) or when cells were in the stationary
and senescent stages of growth. Wetz & Wheeler
(2007) also found PER rates of approximately 5% in
batch cultures of four coastal diatom species:
Cylindrotheca closterium, Odontella longicruris,
Bellerochea sp., and Skeletonema sp. However, PER
for Chaetoceros decipiens was higher, at 21%. López-
Sandoval et al. (2013) measured DOC release using
14
C as a tracer in two-hour incubations using samples
from non-axenic batch cultures. Their comprehensive
survey of 22 species ranged in size from the small
cyanobacterium Prochlorococcus sp. (0.12 µm3
cell volume) to the large diatom Coscinodiscus wai-
lesii (2 500 000 µm3). Mean PER was approximately
2% with a range of 0.3–10%. Unlike other studies,
they found that both cell size and growth phase had no
effect on DOC release. The chemical composition of
extracellular DOM was shown to be different from
intracellular composition in the diatom Skeletonema
costatum (Granum et al., 2002; Puskaric & Mortain-
Bertrand, 2003), confirming earlier work by Mague
et al. (1980). These observations suggest that DOM
release is not simply the passive leakage of intracel-
lular metabolites into the surrounding medium.
Many phytoplankton are mixotrophic, meaning that
they are able to supplement the organic carbon fixed
via photosynthesis with the heterotrophic consump-
tion and assimilation of organic matter (reviewed by
Caron, 2000). Organic matter may be obtained by
phagotrophy or through the uptake and assimilation
of DOM. For example, some diatoms are able to grow
in the dark on simple organic substrates such as glu-
cose and acetate (Lewin & Lewin, 1960; White, 1974)
and the cyanobacterium Prochlorococcus takes up
amino acids in situ (Zubkov et al., 2004). The uptake
of DOM by phytoplankton has not been accounted for
during laboratory culture experiments to determine
PER. Measured PER may represent ‘net PER’, being
the sum of ‘gross PER’ and the subsequent re-uptake
of a proportion of the PER by the phytoplankton
(Kamjunke & Tittel, 2009). This may seem a very
inefficient way to retain resources; however, it may
22
cost the organism less to take up a proportion of the
DOM that has leaked from the cell rather than to
prevent the leakage in the first place. While differen-
tiating between gross and net PER may be important
for understanding the physiology of phytoplankton, it
could be argued that only net PER matters ecologi-
cally as it is only net PER that is available to other
organisms in the surrounding water.
PER in mesocosm experiments and natural waters
Baines & Pace (1991) determined PER based on data
from both marine and freshwater systems in 16
papers. The range of measured PER was < 1 to 75%,
with the means for individual systems ranging from 3
to 40%. They concluded that PER averages 13% and
extracellular release increases linearly with particulate
primary productivity. Nagata (2000) also reviewed the
literature on DOM exudation in the field and con-
cluded that there is a great variation in rates, with
mean PER usually in the range 10–20%. These con-
clusions broadly agree with Baines & Pace (1991).
While there has been limited work on phytoplankton
in monocultures since Nagata (2000), researchers
have continued to measure PER in situ or in large-
scale manipulative experiments with natural commu-
nities in mesocosms (Table 1). Most of the research to
date has focused on coastal waters; the lack of data
from oceanic biomes means that it is difficult to make
global generalizations concerning PER from these
analyses. There has been a geographical bias towards
certain oceans that largely reflects the locations of the
scientists studying DOM production by phytoplank-
ton. Thus, there is a significant body of work on the
Atlantic Ocean and Mediterranean Sea, while rela-
tively little work has been done on the Arctic, Pacific
and Indian Oceans.
PER rates in the field are consistently higher than
rates measured with laboratory monocultures of phy-
toplankton. This may reflect physiological con-
straints. For example, the early stages of batch
cultures are likely to be nutrient replete, whereas nat-
ural waters are often nutrient limited. However, this is
not the only factor, as PER is also generally higher in
situ at upwelling locations, where nutrients are avail-
able, compared with laboratory monocultures. Short-
term incubations using water collected in situ include
protozoan grazing and viral lysis, processes that are
usually absent in phytoplankton cultures (Nagata,
2000; Teira et al., 2001a). In low biomass locations,
such as the oligotrophic ocean, methodological con-
straints may lead to an overestimation of PER based
on incubations using 14C, as the signal is relatively
low compared with the noise, and this may be a con-
cern in the interpretation of some of the early measure-
ments (Williams, 1990). It is difficult to compare the
in situ studies presented in Table 1 due to the wide
range of protocols used to obtain the data. For
Table 1. Field measurements of DOM release by phytoplankton, expressed as percentage extracellular release (PER). Measurements of PER are means unless stated otherwise under notes. Data are
taken from papers published since 2000 and grouped according to which ocean the measurements were made in.

Author Location Season PER (%) Notes

Phytoplankton DOM release

Arctic
Engel et al. (2013) Arctic, Kongsfjorden Summer 14 ± 8 Mean ± standard deviation in a fjord in Spitsbergen, Svalbard
Atlantic Ocean
Teira et al. (2001a) Atlantic, N. subtropical gyre Summer/autumn 11–42 Oligotrophic waters
Teira et al. (2001a) Atlantic, coastal upwelling Summer/autumn 4–9 Benguela upwelling (Mauritania) and upwelling off NW Spain
Teira et al. (2001b) Atlantic, Iberian upwelling Summer/autumn > 15 Picoplankton dominated; net heterotrophic
Teira et al. (2001b) Atlantic, Iberian upwelling Summer/autumn < 10 Coastal upwelling, cells > 2 µm diameter; net autotrophic
Morán et al. (2002a) Atlantic Spring 10.3 Coastal waters
Morán et al. (2002a) Atlantic Spring 8.4 Offshore waters
Morán et al. (2002a) Atlantic Summer 6.8 Coastal waters
Morán et al. (2002a) Atlantic Summer 6.1 Offshore waters
Teira et al. (2003a) Atlantic, Iberian upwelling All seasons 37 Highest rates during periods of lowest productivity
Teira et al. (2003b) Atlantic, N. subtropical gyre Summer 20 Cell lysis and grazing more important than exudation
Marañón et al. (2004) Atlantic, Ría de Vigo All seasons 19 Coastal upwelling ecosystem
Marañón et al. (2005) Atlantic, Celtic Sea Summer c. 20 Productivity gradient from oligotrophic to euphotic waters
López-Sandoval et al. (2010) Atlantic, Ría de Vigo All seasons 19 14% during exponential growth and 23% during senescence
Mediterranean Sea
Morán & Estrada (2001) Mediterranean, Alboran Sea Early summer 4–44 PER range at three sites
Lagaria et al. (2011) Mediterranean Summer 9.2, 15.2, 17.7 Mean values in 3 oligotrophic anticyclonic gyres
López-Sandoval et al. (2011) Mediterranean Summer 37 Productivity gradient in stratified waters
Pacific Ocean
Wetz & Wheeler (2003) Pacific, coastal off Oregon Summer 38 Chaetoceros sp. bloom during coastal upwelling
Wetz & Wheeler (2003) Pacific, coastal off Oregon Summer 15 Leptocylindricus minimus during coastal upwelling
Southern Ocean
Morán et al. (2001) Southern, Weddell & Scotia Seas Summer 13 Range 5–33%
Morán & Estrada (2002) Southern, Antarctic Peninsula Summer 24 Range 2–47%
23
D. C. O. Thornton
example, Wetz & Wheeler (2003) conducted on-deck
incubations of 20 litres, which were sampled each day
for 7 days, whereas Teira et al. (2001a) measured
DOC release in 30-ml samples after an on-deck incu-
bation time of 2 hours. These differences suggest that
an inter-comparison of methods commonly used to
measure PER would be a valuable exercise, poten-
tially leading to a standard protocol and enabling
direct comparisons between datasets collected by dif-
ferent groups at different times and locations.
In summary, PER is generally relatively low
(10–20%) in nutrient-rich conditions, such as coastal
upwelling, and frequently higher in warm, nutrient-
poor conditions such as the North Atlantic subtropical
gyre during summer. The phytoplankton that grow
under these different conditions are also very differ-
ent; coastal upwelling zones are dominated by large
taxa and subtropical gyres are dominated by small
taxa with large surface area to volume ratios. This is
consistent with Fogg (1983), who concluded that
phytoplankton exude 5% of the products of photo-
synthesis in eutrophic waters and up to 40% in oligo-
trophic waters.
PER in biogeochemical models
DOM release by phytoplankton is a potentially
important component of biogeochemical models
on a variety of spatial and temporal scales, from
ecophysiological models of individual phytoplank-
ton cells, to ecosystem models and models of global
biogeochemical cycles. Empirical and mechanistic
methods have been used to incorporate phytoplank-
ton DOM exudation into models.
The simple empirical approach is to assume a fixed
value for PER, based on averaging data from measure-
ments in the field or laboratory. The value for PER is
then multiplied by a measure of primary production to
estimate the amount of DOM produced. This
approach has been used in multiple studies, as tabu-
lated by Christian & Anderson (2002), with values of
PER generally around 5%. Aumont et al. (2003)
incorporated fixed values of DOC release into their
ecosystem model of the global ocean containing two
functional phytoplankton groups. DOC release was
fixed at 5 and 3% for nanophytoplankton and diatoms,
respectively. Recently, PER in the upper Chesapeake
Bay was assumed to be a constant 26% (Keller &
Hood, 2011), a relatively high value that seems to be
based on a misinterpretation of Anderson & Williams
(1998).
Using the mechanistic approach, DOC release by
phytoplankton is incorporated into models as a
dynamic term that changes in response to environ-
mental conditions. PER has been modelled using cell
quotas (Baklouti et al., 2006) or N : C ratios (Flynn
et al., 2008) as a measure of nutrient status. Kriest &
Oschlies (2007) modelled the effect of cell size on
24
DOC release based on Bjørnsen’s (1988) model,
which assumes that DOC release by phytoplankton
is a passive process driven by concentration gradients
across the cell membrane. In this model, small cells
leak more than large cells and therefore the size spec-
trum of the phytoplankton population was a driver of
DOC release (Kriest & Oschlies, 2007). The advan-
tage of the mechanistic approach is that it implies an
understanding of the physiological factors that affect
DOC exudation by phytoplankton and therefore it can
be used predictively to model situations where PER
measurements are lacking.
Anderson & Williams (1998) combined the empiri-
cal and mechanistic approaches to estimate PER in
their model of DOM cycling in the English Channel.
They divided DOC lost from phytoplankton cells into
two components. Firstly, a constant 5% of carbon
fixed by the phytoplankton was lost by leakage from
the cells. Leakage was defined as the passive loss of
‘small molecules’ across the cell membrane.
Secondly, they distinguished ‘leakage’ from ‘exuda-
tion’, which was defined as the loss of excess carbon
due to changes in environmental conditions such as
light and nutrient availability. The exudation contribu-
tion to extracellular DOC was calculated using two
different methods: it was either simply directly pro-
portional to primary production or it was calculated as
a photosynthetic overflow under conditions of nutrient
limitation. Total PER was calculated accounting for
both leakage and exudation. Mongin et al. (2003) used
a similar approach, assuming that 10% of the phyto-
plankton biomass was passively leaked from the cells
each day, with DOC and DON released in Redfield
stoichiometry, plus a further leakage of DOC and
DON released in Redfield stoichiometry equivalent
to 5% of the inorganic nitrogen uptake each day. In
addition, when C : N > 10, 30% of the photosyntheti-
cally fixed carbon was exuded as DOC to simulate
exudation under nitrogen limitation.
The success of DOM release models will depend on
accurate predictions over a wide range of naturally
occurring conditions, enabling them to be incorpo-
rated into larger models of global primary production
and biogeochemical cycles. Currently, the models
reflect our lack of understanding of the basic physiol-
ogy of DOM release by phytoplankton and associated
physiological processes, such as cell death (see
below). Mechanistic models at least enable us to iden-
tify what probably drives DOM release by phyto-
plankton, even if the relative importance of the
different processes is currently difficult to determine.
Drivers of DOM release in mechanistic models
include photosynthesis rates, cell quotas and elemen-
tal stoichiometry, concentration gradients across the
plasma membrane, cell size, growth rates, and cell
death (Baklouti et al., 2006; Kriest & Oschlies,
2007; Flynn et al., 2008). However, because the dri-
vers of DOM release by phytoplankton are poorly
Phytoplankton DOM release
characterized, it is possible to tune models to fit data
without realizing that the resulting model is unrealis-
tic. Flynn et al. (2008) concluded that suitable data to
model DOM release limit our mechanistic understand-
ing of the process. The ideal data, which Flynn et al.
(2008) were unable to find in the literature, should
demonstrate mass balance of carbon (or nitrogen). In
the case of carbon, this would mean simultaneous
measurements of dissolved inorganic, dissolved
organic and particulate carbon fractions under con-
strained axenic conditions, to enable a budget of car-
bon to be constructed with no assumed pools (Flynn
et al., 2008). There is a need for integrated research,
specifically designed to combine modelling with
experimental work on phytoplankton physiology.
Composition of DOM released by phytoplankton
Phytoplankton release a broad range of organic com-
pounds. Lancelot (1984) summarized the early litera-
ture on the composition of DOM released by
phytoplankton, concluding that they were dominated
by carbohydrates (monosaccharides, oligosaccharides
and polysaccharides), nitrogenous compounds (amino
acids, polypeptides and proteins), lipids (fatty acids)
and organic acids (glycolate, tricarboxylic acids,
hydroxamate and vitamins). As one might expect,
this broadly matches the composition of phytoplank-
ton cells. A typical phytoplankter is composed of
25–50% protein, 5–50% polysaccharide, 5–20%
lipids, 3–20% pigments and 20% nucleic acids
(Emerson & Hedges, 2008). Hellebust (1974) grouped
the extracellular products of algae (both phytoplank-
ton and macroalgae) into the following categories:
carbohydrates, nitrogenous substances, organic acids
(mainly glycolate), phenolic substances, organic
phosphates, volatile substances, enzymes, vitamins,
sex factors, growth inhibitors and stimulators, and
toxins. This list includes categories determined on
the basis of their chemical composition (e.g. carbohy-
drates and nitrogenous substances), their chemical
properties (volatile substances) and their biological
function (e.g. enzymes and sex factors). Grouping
extracellular products in this way is confusing, as
there is overlap between categories; for example,
enzymes are nitrogenous substances as well. I have
grouped the extracellular products based on chemical
composition, either in broad encompassing categories
(e.g. carbohydrates) or by specific compounds (e.g.
isoprene). The list is not exhaustive, but rather repre-
sents categories or compounds which are either extre-
mely abundant or biogeochemically significant.
Amino acids and proteins
The extracellular release of amino acids, peptides and
proteins by phytoplankton has not been extensively
studied. Field (Bronk et al., 1994; Glibert & Bronk,
25
1994; Hu & Smith, 1998) and culture (Suratman et al.,
2008) studies have shown that a range of phytoplankton
taxa release a significant amount of dissolved organic
nitrogen (DON). Many phytoplankton are also consu-
mers of DON as a nitrogen source; it is often the largest
pool of dissolved nitrogen in marine waters and it is less
refractory than once thought (Bronk et al., 2007). Given
that protein is a major component of phytoplankton, it is
likely that amino acids and protein form a significant
proportion of the DON released.
Work with cultures of diatoms has shown that
Chaetoceros spp. (Poulet & Martin-Jézéquel, 1983;
Myklestad et al., 1989) and Skeletonema costatum
(Mague et al., 1980; Granum et al., 2002) release
amino acids into the growth medium. Myklestad
(2000) concluded, based on the literature, that the
following amino acids are commonly released by
diatoms: serine, glycine, lysine, alanine, glutamic
acid, aspartic acid, ornithine and histidine. Larger
amino acid-containing molecules may be released by
phytoplankton. For example, Thalassiosira weissflo-
gii grown at several copper concentrations released
the tripeptide glutathione (GSH) in response to cop-
per-induced cell membrane damage (Tang et al.,
2005). Emiliana huxleyi released thiols composed of
the amino acids arginine, cysteine and glutamine in
response to heavy metals (Dupont et al., 2004).
Amino acids containing R-groups with aromatic car-
bon rings, and consequently delocalized electrons, are
fluorescent. Common amino acids containing such R-
groups are tryptophan, phenylalanine, and tyrosine
and so these amino acids, and proteins that contain
them, contribute to the fluorescent dissolved organic
matter (FDOM) pool in the ocean (Coble, 1996). The
concentration of ‘proteinaceous DOM’, determined
using fluorescence, increased in mesocosms during
phytoplankton exponential growth (Stedmon &
Markager, 2005). Chaetoceros, Skeletonema,
Prorocentrum and Micromonas all released ‘protein-
like’ FDOM during culture experiments (Romera-
Castillo et al., 2010). In addition, small protein-con-
taining exopolymer particles are abundant in the
ocean. These particles are known as Coomassie stain-
ing particles (CSP) after Coomassie Brilliant Blue G-
250 dye, which is the protein stain used to detect them
(Long & Azam, 1996). Data from my laboratory has
shown that CSP are a ubiquitous component of the
exopolymers produced in diatom cultures (Figs 1, 2)
and the ocean (Fig. 3).
Carbohydrates
Carbohydrates are used in the structural compo-
nents of the cell, such as cell walls, and as storage
compounds for fixed carbon and energy. The com-
position and amount of carbohydrate that an indivi-
dual phytoplankton cell contains are dependent on
the physiological status of the cell and its taxonomic
D. C. O. Thornton 26

Fig. 1. Coomassie staining particle (CSP) concentration in diatom batch cultures at the end of the exponential growth phase after
7 days of growth in artificial seawater. The diatoms were Skeletonema marinoi (SM), Skeletonema costatum (SC), Phaeodactylum
tricornutum (PT), Chaetoceros muelleri (CM), Coscinodiscus wailesii (CW), Odontella aurita (OA) and Achnanthes longipes (AL).
Bars show mean + SD (n = 3 replicate cultures). Data collected by Michael Pohlen. CSP stained according to Long & Azam (1996).

2 3

4 5

Figs 2–5. Exopolymer particles observed in diatom cultures and the Pacific Ocean. Exopolymer particles were collected using gentle
filtration onto 0.4 µm polycarbonate filters and stained. 2. Coomassie brilliant blue staining particles (CSP) in a culture of
Thalassiosira weissflogii. 3. CSP particles from the surface Pacific Ocean collected off the coast of Oregon during July 2011. 4.
Transparent exopolymer particles (TEP) in a culture of Thalassiosira weissflogii. 5. TEP particles from the surface Pacific Ocean
collected off the coast of Oregon during July 2011. TEP were stained with Alcian blue according to Alldredge et al. (1993) and CSP
were stained according to Long & Azam (1996). Scale bars = 100 µm.

affiliation. Carbohydrates are a significant compo-
nent of the DOM in the ocean (Aluwihare et al.,
1997; Repeta & Aluwihare, 2006; Hansell et al.,
2009).
Data indicate that different species produce differ-
ent extracellular carbohydrates, in terms of monosac-
charide composition and their relative proportions. It
is probable that an individual phytoplankton strain or
species is capable of producing multiple extracellular
carbohydrates at the same time. This has been shown
for benthic diatoms, whose extracellular carbohydrate
production has been extensively studied over the last
few years (Underwood & Paterson, 2003; Bellinger
et al., 2005, 2009; Abdullahi et al., 2006).
Monosaccharides commonly found in extracellular
carbohydrates released by marine phytoplankton
include aldohexoses (glucose, galactose and man-
nose), aldopentoses (arabinose and xylose), deoxysu-
gars (fucose and rhamnose), uronic acids (glucuronic
acid) and amino sugars (Aluwihare et al., 1997;
Biersmith & Benner, 1998; Aluwihare & Repeta,
1999; Magaletti et al., 2004; Kragh & Søndergaard,
2009). The monosaccharide composition of the sur-
face ocean is similar to the monosaccharide composi-
tion of phytoplankton extracellular release, indicating
that phytoplankton are a major source of
Phytoplankton DOM release
carbohydrates to the ocean (Aluwihare et al., 1997;
Biersmith & Benner, 1998).
Over the last two decades there has been consider-
able interest in the role of large polymers in the ocean
(see reviews by Passow, 2002a; Verdugo et al., 2004;
Verdugo, 2012). There has been the realization that
there is a continuum of organic matter from DOM to
POM, with gels and exopolymer particles sharing
some of the properties of both POM and DOM.
Verdugo et al. (2004) estimated that 10% of the
DOM pool, or approximately 70 Pg C, is in the
form of biopolymers that are assembled into gels
such as transparent exopolymer particles (TEP).
TEP are operationally defined as particles retained
on 0.4 µm (or sometimes 0.2 µm) pore sized poly-
carbonate filters that stain with Alcian blue (Figs 4,
5) (Alldredge et al., 1993; Passow & Alldredge,
1995; Passow, 2002a). TEP are invisible using
bright-field light microscopy, but become visible
after staining, indicating that TEP contain acid poly-
saccharides (Ramus, 1977; Passow & Alldredge,
1995). TEP are ubiquitous and play an important
role in particle dynamics and carbon cycling in the
ocean (see reviews by Passow, 2002a; Burd &
Jackson, 2009; Verdugo, 2012). For example, TEP
are sticky and affect the further aggregation of parti-
cles into larger aggregates that sink rapidly though
the water column, affecting the biological carbon
pump (Engel, 2000; Passow, 2002a; Thornton,
2002). Exudation by phytoplankton plays a signifi-
cant role in the formation of TEP (Passow, 2002b;
Gärdes et al., 2011). Numerous studies have shown
that exopolymer particles accumulate in phytoplank-
ton cultures (Passow, 2002b; Claquin et al., 2008;
Fukao et al., 2010) and during blooms (Passow et al.,
1994; Engel et al., 2002; Engel, 2004; Harlay et al.,
2009) (Figs 3, 5). Generally, TEP are not exuded
directly by phytoplankton cells; they form abiotically
from precursors released by cells. TEP accumulate in
0.2 µm filtrate from diatom cultures that is bubbled
with air (Mopper et al., 1995; Mari, 1999) or exposed
to fluid shear (Passow, 2000); therefore processes
that bring the polymeric precursors together affect
the formation of TEP.
Fatty acids and lipids
Myklestad (2000) noted that there was little informa-
tion on the exudation of fatty acids and lipids by
phytoplankton, and there has been little further research
on this issue over the last decade. Parrish (1987)
hypothesized that dissolved lipids he measured in
Bedford Basin (Canada) were exuded by phytoplank-
ton during the spring bloom. There has been some
work on extracellular lipid production by marine dia-
toms grown in continuous culture (Parrish &
Wangersky, 1987; Lombardi & Wangersky, 1991).
Chaetoceros gracilis produced extracellular lipids
27
under nutrient-replete conditions and also under condi-
tions of phosphorus and silicon limitation (Lombardi &
Wangersky, 1991). Similarly, Phaeodactylum tricornu-
tum produced extracellular lipids under both nitrogen-
limited and nitrogen-replete conditions (Parrish &
Wangersky, 1987). Extracellular free fatty acids, tria-
cylglycerols, sterols, phospholipids and glycolipids
were measured in cultures of the dinoflagellate
Gymnodinium cf. nagasakiense and were proposed to
be exuded from the cells (Parrish et al., 1994).
Nucleic acids
There is little information on dissolved nucleic acids
in the ocean and no specific information on the
potential for phytoplankton to exude nucleic acids.
The viral lysis of bacterioplankton is known to be a
significant source of dissolved DNA (Brum, 2005;
Riemann et al., 2009). Most of the nucleic acids in
eukaryotic cells are large molecules contained within
membrane-bound organelles, which will reduce the
potential for leakage as each membrane will act as a
barrier. Nucleic acids are rich in phosphorus and
nitrogen and therefore the loss of significant amounts
of nucleic acid would be costly to phytoplankton
cells, which inhabit environments where nitrogen
and phosphorus often limit growth. Based on these
arguments, it seems unlikely that nucleic acids are a
significant source of DOM produced by healthy phy-
toplankton cells. However, recent work has shown
that extracellular DNA (eDNA) plays a significant
structural role in the exopolymer matrix of many
bacterial biofilms (reviewed by Flemming &
Wingender, 2010). This raises the possibility that
eDNA may be exuded by phytoplankton that
produce large amounts of exopolymers, such as dia-
toms and the colonial microalga Phaeocystis.
Dissolved DNA supplied 70% of bacterioplankton
P demand in a P-limited estuary, indicating that
eDNA may play a significant role in some ecosys-
tems (Riemann et al., 2009).
Glycolate
Glycolate (C2H4O3) is produced during photorespira-
tion (Falkowski & Raven, 2007). Much of the early
work on DOM release by phytoplankton was focused
on glycolate (also known as glycollate, glycolic acid
or 2-hydroxyethanoic acid), mainly in freshwater
model taxa such as Chlorella (Tolbert & Zill, 1956;
Whittingham & Pritchard, 1963). Leboulanger et al.
(1998a) proposed that glycolate may represent 10% or
more of the DOC in the ocean, though data to support
this estimate were not presented. Concentrations vary-
ing between 0.20 and 0.80 µM were measured in
coastal waters of the Irish Sea (Liverpool Bay) (Al-
Hasan & Fogg, 1987). Leboulanger et al. measured
glycolate concentrations up to 0.97 µM in
D. C. O. Thornton
mesotrophic waters and 0.22 µM in oligotrophic
waters of the tropical Atlantic Ocean (Leboulanger
et al., 1997), and 0.32–1.17 µM during a phytoplank-
ton bloom in coastal Mediterranean waters
(Leboulanger et al., 1994). Relatively high glycolate
concentrations (0.89–4.50 µM) have been measured
in coastal waters off Belgium (Billen et al., 1980). It is
likely that there is rapid turnover of the glycolate pool
in the ocean due to production associated with photo-
synthesis and consumption by heterotrophic prokar-
yotes. This is shown by the diurnal cycle in glycolate
concentrations in the upper ocean, indicating net pro-
duction during daylight and net consumption during
the night (Leboulanger et al., 1997, 1998b).
Dimethylsulfoniopropionate (DMSP) and
dimethysulfide (DMS)
The production of DMS (C2H6S) and its precursor
compound DMSP (C5H10O2S) by phytoplankton has
been studied extensively over the last 25 years. Early
research focused on the production of DMS, as it is the
major source of non-sea salt aerosol over areas of
ocean remote from the continents (Stefels & van
Boekel, 1993; Gondwe et al., 2003), it affects cloud
formation and has a hypothetical role in climate reg-
ulation (Charlson et al., 1987; Ayers & Cainey, 2007;
Quinn & Bates, 2011). However, recent research has
focused on DMSP, which is often a significant com-
ponent of the carbon quota of phytoplankton cells and
may play a significant role in prokaryote production
and the microbial loop (Kiene et al., 2000). Major
determinants of DMSP and DMS concentrations in
the ocean are phytoplankton biomass and community
composition (Malin et al., 1998). Representatives
from most of the major phylogenetic groups of eukar-
yote phytoplankton are known to produce DMSP
(Malin & Kirst, 1997). Simó et al. (2002) found that
DMSP synthesis was proportional to photosynthesis
in the North Atlantic and that phytoplankton invested
7% of net primary production into DMSP production.
Compiling data from a range of in situ experiments
and culture work, Kiene et al. (2000) concluded that
DMSP forms <1 to 39% of the cell carbon quota of
phytoplankton, with most values lying in the range of
1–5%. Dissolved DMSP concentrations in surface
waters were in the range 0.1–25 nM, with a turnover
rate of 0.3–129 nM day–1 (Kiene et al., 2000). DMS
production was associated with high in situ phyto-
plankton productivity during the Southern Ocean
Iron enrichment Experiment (SOFeX). In a patch of
water in which productivity was stimulated by the
addition of the limiting nutrient iron, the mean (±
SD) DMS concentration was 7600 ± 480 pptv, com-
pared with 1560 ± 90 pptv outside the fertilized patch
(Wingenter et al., 2004).
28
The physiological functions of DMSP and DMS are
uncertain, though they may be components of an
intracellular antioxidant system (Sunda et al., 2002).
The release of DMSP and DMS generally depends on
processes that disrupt cell integrity, rather than exuda-
tion by healthy cells (Kiene et al., 2000). Examples
include senescence, grazing (Wolfe & Steinke, 1996;
Wolfe et al., 1997) and viral lysis (Malin et al., 1998).
However, a modelling study estimated that
Prorocentrum minimum (a dinoflagellate) exudes 1%
day−1 of its cell quota of DMSP, whereas Phaeocystis
sp. (a prymnesiophyte) exudes from 3 to 11% day−1 of
its cell quota of DMSP (Laroche et al., 1999). Given
that the DMSP concentration in Phaeocystis sp. cells
is 71–150 mM (Stefels & van Boekel, 1993) and that
DMSP may form a significant component of the car-
bon cell quota, the exudation or leakage of even a
small proportion of cell DMSP may be a significant
source of DOM during phytoplankton blooms of high
DMSP producing species.
Isoprene
Shaw et al. (2003) grew a range of phytoplankton
species and found that they all produced isoprene
(2-methyl-1,3-butadiene, an alkene with the formula
C5H8) during exponential growth in laboratory cul-
tures. The range of isoprene production rates were
between 1 × 10−21 and 4 × 10−19 mol cell–1 day−1.
Shaw et al. (2003) also measured the production of a
range of light non-methane hydrocarbons (C2 to C6);
however, only isoprene was consistently produced by
the five phytoplankton species studied. Bonsang et al.
(2010) grew a range of phytoplankton species, repre-
senting different major phylogenetic groups (cyanobac-
teria, diatoms, coccolithophores and chlorophytes), in
laboratory cultures. All the phytoplankton investigated
emitted isoprene, with the highest production rates (per
unit chlorophyll a) occurring in the cyanobacteria
(Trichodesmium and Synechococcus) and the lowest
in the chlorophyte Dunaliella tertiolecta. Isoprene pro-
duction was also shown to be elevated in waters ferti-
lized with iron during the SOFeX experiment
(Wingenter et al., 2004). Mean (± SD) isoprene con-
centration was 560 ± 13 pptv in the fertilized patch,
compared with 139 ± 6 pptv outside the patch in
unfertilized water (Wingenter et al., 2004). Recent esti-
mates of isoprene flux from ocean to atmosphere are
0.11–1.9 Tg isoprene year−1 (Palmer & Shaw, 2005;
Arnold et al., 2009).
Why do phytoplankton produce extracellular
DOM?
John Sharp (1977) originally posed the question
‘Excretion of organic matter by marine phytoplank-
ton – do healthy cells do it?’ as the title of a well-cited
Phytoplankton DOM release 29

paper. It was his contention that the observed release
(which he called ‘excretion’) of DOM by phyto-
plankton was a methodological artefact arising from
the 14C tracing methods used to determine photo-
synthesis rates and DOM production. He identified
several potential problems that could lead to over-
estimates of DOM release by phytoplankton, includ-
ing residual inorganic 14C contamination in the
medium and the rupture of cells during filtration.
Data over the last 35 years have convincingly
answered Sharp’s (1977) question and demonstrated
that healthy phytoplankton do release DOM.
Considerable progress has been made in determining
the composition and amount of DOM released
by phytoplankton. However, the next logical ques-
tion – Why do healthy phytoplankton release dis-
solved organic matter? (Bjornsen, 1988) – has not
been adequately addressed. Generally, DOM
released by phytoplankton can be divided into two
categories: compounds that have specific functions
(e.g. extracellular enzymes, siderophores and toxins)
and compounds that have no known function. It is the
production of the latter that dominates phytoplankton
DOM release (Nagata, 2000). The release of DOM
has a cost in terms of resources lost (fixed carbon and
energy), which implies that the release of the major-
ity of DOM must either have a negligible impact on
the phytoplankton or have an unknown function.
Figure 6 summarizes the major mechanisms that
may account for the loss of fixed carbon by phyto-
plankton through DOM release. These mechanisms
are not mutually exclusive; it is likely that an indivi-
dual organism will lose fixed carbon through multi-
ple mechanisms simultaneously. However, not all
mechanisms will apply to all phytoplankton all of
the time.
DOM release by phytoplankton is the sum of leak-
age across the cell membrane and active exudation,
with the relative balance of these two processes
depending on the physiological status of the cell. In
Fig. 6, leakage is defined as any passive loss of DOM
from the cell, including losses associated with defined
processes (such as the diffusive loss of recent photo-
synthates) and a general loss by passive diffusion.
While passive diffusion is constant, other processes
associated with leakage and all active exudation pro-
cesses will vary in response to environmental factors
such as nutrient availability. For example, one could
hypothesize that the loss rate of DOM across the cell
membrane via passive diffusion is relatively constant
in a healthy cell, whereas the loss of organic carbon
associated with photorespiration will depend on
photosynthetic activity, which in turn will depend on
environmental factors such as light availability and
temperature. Under such a scenario, the proportion
of total DOM lost due to passive diffusion would be
greater during the night than during daylight. The
balance of low molecular weight and high molecular
weight DOM released by the cell will depend on the
relative proportions of DOM released through leakage
or exudation. The DOM released through leakage will
tend to be dominated by small, uncharged molecules
that can easily pass through cell membranes, whereas
exudates are often dominated by large polymers that
do not diffuse across the cell membrane (Baines &
Pace, 1991; Myklestad, 2000). At present, there is no
method to directly measure the contributions of leak-
age and exudation to total DOM release.
Consequently, the relative contribution of these pro-
cesses is inferred, often on the basis of indirect evi-
dence, such as the size of the molecules released.
DOM release by passive diffusion across the cell
membrane
There is a 106 times increase in DOM concentration
moving across the cell membrane from the external
environment into the cell (Flynn et al., 2008). This

leakage exudation / leakage

Passive diffusion Photosynthetic overflow
A
B
exudation leakage / exudation
H
Density reduction Autocatalytic cell death
C
Phytoplankton
exudation exudation/ leakage
G
infochemicals Photorespiration
D
F E
exudation exudation
Defence mechanisms Resource acquisition

Fig. 6. Mechanisms affecting the release of dissolved organic matter (DOM) from phytoplankton cells via leakage and exudation.
Leakage is passive loss, while exudation is the active transport of DOM to the environment outside the cell. A. Passive diffusion
losses driven by the concentration gradient across the cell membrane and membrane permeability. B. Removal of excess carbon fixed
during photosynthesis by photosynthetic overflow. C. Loss of cell membrane integrity during autocatalytic cell death. D. Loss of
glycolate from the cell during photorespiration. E. Exudation of exoenzymes and siderophores used in the acquisition of nutrients.
F. Exudation of compounds as chemical defense against predators or infectious agents. G. Exudation of molecules that carry
information between organisms. H. Exudation of polymers which stick to the surface of the cell and reduce sinking rates by density
reduction or increasing frictional resistance.
D. C. O. Thornton
concentration gradient is the major factor that drives
the passive leakage of DOM from phytoplankton
cells. Factors affecting the rate of DOM leakage by
diffusion across the cell membrane are cell permeabil-
ity, surface area to volume ratio of the cell, and the size
of the intracellular pool of the compound in question
(Bjørnsen, 1988):
E A
’P (1)
S V
Where E is leakage rate of a compound by diffusion
(mol s−1), S is the intracellular pool of the compound
(mol), P is cell membrane permeability (cm s−1), A is
cell surface area (cm2), and V is cell volume (cm3)
(Bjørnsen, 1988). As equation 1 shows, the surface
area to volume ratio of the cell, and therefore cell size,
is an important determinant of how much DOM is lost
via diffusion. Consequently, Bjørnsen (1988) argued
that this passive loss of DOM was analogous to a
‘property tax’ on phytoplankton biomass rather than
an ‘income tax’ determined by primary productivity.
Cell membranes are more permeable to uncharged low
molecular weight compounds, therefore the passive
loss of DOM from phytoplankton will be dominated
by small molecules such as urea. Work with synthetic
lipid bilayers shows that membrane permeability to
ions (e.g. H+) < large uncharged polar molecules (e.g.
sucrose) < small uncharged polar molecules (e.g. H2O
and urea) < hydrophobic molecules (e.g. O2) (Alberts
et al., 2008). Bjørnsen’s (1988) use of the word ‘tax’
implies a direct cost to the organism; the significance
of this cost is not known.
Subsequent work has both supported and contra-
dicted the passive diffusion model of DOM release.
For example, Baines & Pace (1991) concluded that
DOM release is constrained by the total availability of
photosynthates, rather than phytoplankton biomass,
and therefore active processes are more important
than diffusion. However, constant PER throughout
the water column, which only increased at very low
light conditions, led to the conclusion that DOC
release was the result of passive diffusion rather than
photosynthetic overflow (Marañón et al., 2004, 2005).
The passive diffusion model implies that a population
dominated by small cells should have a higher PER
than populations of larger cells. Measurements of
DON release using 15NH4+ as a tracer in two size
fractions (< 94 µm and < 20 µm) of natural phyto-
plankton showed that the smallest size fraction had the
greatest PER with respect to organic nitrogen, though
the amount of DON released was greatest in the
fraction containing large cells (Hasegawa et al.,
2000). This reiterates that while PER is a useful con-
cept, it does not give any information about the mag-
nitude of the DOM release (Mague et al., 1980;
Williams, 1990).
30
Overflow hypothesis
DOM exudation as a consequence of excess carbon
being fixed by photosynthesis (Fig. 6) is frequently
invoked as the major mechanism to explain DOM
release by phytoplankton. Like passive diffusion, the
loss of DOM from photosynthetic overflow is gener-
ally regarded as a consequence of inefficiencies in cell
physiology with the extracellular products serving no
function outside the cells. The release of photo-
synthate under conditions of high light (Hellebust,
1965; Zlotnik & Dubinsky, 1989) and nutrient scarcity
may be an overflow mechanism when photosynthesis
occurs more rapidly than is required for growth (Fogg,
1983; Wood & Van Valen, 1990). For example, if a
cell is growing under conditions of nitrogen limitation
there will be insufficient nitrogen to support growth of
the cell, which requires the synthesis of proteins,
nucleic acids and other nitrogen-containing com-
pounds. Equally, there may not be enough available
nitrogen to ‘switch off’ photosynthesis, as this would
require the synthesis of proteins and nucleic acids to
reorganize the photosynthetic apparatus. After the
carbohydrate storage capacity of the cell is exceeded,
the excess organic carbon is exuded from the cell. As
light and usable inorganic carbon sources are readily
available under this scenario, the strategy has little or
no cost to the phytoplankter.
Batch culture experiments have shown that phyto-
plankton release more DOM under conditions of nutri-
ent limitation (Guillard & Wangersky, 1958; Marker,
1965; Myklestad, 1974, 1977; Obernosterer & Herndl,
1995). Myklestad (1995) concluded that phytoplankton
release carbohydrates into the surrounding medium
under conditions of severe N or P limitation, as carbo-
hydrates do not contain these potentially limiting nutri-
ents. Myklestad et al. (1989) found that the rates of
release of carbohydrates and amino acids by
Chaetoceros affinis were highest in the growth phase
compared with stationary phase batch cultures.
However, the photosynthesis rate of nutrient-limited
cells was lower and therefore DOM release accounted
for 58% of productivity in stationary phase cells, com-
pared with 10% during exponential growth. It is
assumed that the accumulation of DOM in phytoplank-
ton cultures indicates the uncoupling of growth and
photosynthesis. This is supported by the observation
that the greatest release of DOM occurs during the
transition between different phases of phytoplankton
growth (Granum et al. 2002; Wetz & Wheeler, 2007),
which was explained by Williams (1990) as a ‘tempor-
ary loss of control’ of the organic matter pools within
the cell as growth rate slows down. It is rarely consid-
ered that other processes, such as phytoplankton cell
death resulting in lysis (Franklin et al., 2006), may also
affect the release of DOM in batch cultures. In addition,
there may be taxonomic differences: Skeletonema cost-
atum and Phaeocystis sp. have relatively constant DOC
Phytoplankton DOM release
release rates (which fits the passive diffusion model of
DOM release), whereas Synechococcus bacillaris and
Emiliania huxleyi release more DOC during the sta-
tionary phase (which fits the overflow hypothesis)
(Biddanda & Benner, 1997).
If the overflow hypothesis is applicable, then it is
probable that once the cell content (the cell quota:
Droop, 1968, 1983) of key nutrients (such as N or P)
drops below a threshold, the excess organic carbon is
exuded from the cell. Alternatively, exudation may
not be dependent on a quota or absolute amount of
limiting nutrient, but rather the stoichiometric ratio of
carbon to potentially limiting nutrients. Most models
of phytoplankton growth use ratios, as nutrient quotas
are normalized to carbon (e.g. Geider et al., 1998;
Sunda et al., 2009). Determining the degree to which
C : N : P stoichiometry of phytoplankton deviates
from the canonical Redfield ratio of 106 : 16 : 1 is
seen as an important step in understanding of the
role of phytoplankton in biogeochemical cycling
(Falkowski, 2000; Geider & La Roche, 2002).
However, the Redfield ratio of 106 : 16 : 1 is a mean
C : N : P ratio for marine organic matter and there are
significant differences in the C : N and C : P ratios in
different phyla of phytoplankton (Geider & La Roche,
2002; Quigg et al., 2003). Variation in the C : N : P
ratios (and indeed the C : X ratios of other nutrients) is
a combination of phylogenetics and the physiological
status of the cells (Geider & La Roche, 2002; Arrigo,
2005). Consequently, it is unlikely that there is a
single threshold value of C : N or C : P ratio, which
if exceeded, would predict exudation as a result of
photosynthetic overflow. This is logical when consid-
ered in the context of the variation in threshold stoi-
chiometric ratios indicating limitation. For example,
the critical N : P ratio indicating the transition between
nitrogen and phosphorus limited growth is generally
higher than the Redfield ratio and varies between 20
and 50 (Geider & La Roche, 2002).
β-1,3-glucan is a carbohydrate storage product of
many diatoms and is used as a carbon source to produce
exopolymers (EPS) by epipelic diatoms (Smith &
Underwood, 1998, 2000). The glucan content of
Chaetoceros affinis increases rapidly during the station-
ary phase in nitrate-depleted batch cultures (Myklestad
& Haug, 1972). Granum et al. (2002) dismissed the
overflow hypothesis as a significant carbon sink and
proposed that excess carbon in nitrogen limited
Skeletonema costatum was stored within the cell as
β-1,3-glucan. However, the storage of excess carbon
within the cell and overflow are not necessarily
mutually exclusive; it may be that overflow occurs
once the storage capacity of the cell has been exceeded.
Photorespiration and glycolate production
The stressful conditions (particularly high light) that
affect photosynthetic overflow may also lead to
31
photorespiration. Glycolate is produced by phyto-
plankton during photorespiration (Tolbert, 1974;
Falkowski & Raven, 2007), and while the majority
of glycolate is metabolized, a proportion is released
into the surrounding environment (Falkowski &
Raven, 2007).
Carbon fixation occurs via a carboxylase reaction
affected by the enzyme ribulose-1,5-bisphosphate car-
boxylase–oxygenase (RuBisCO). Whether RuBisCO
acts as an oxygenase or carboxylase depends on the
kinetics of RuBisCO within the organism and the
steady state concentration of CO2 and O2 (Falkowski
& Raven, 2007). Photorespiration is affected by the
oxygenase activity of the enzyme, leading to the pro-
duction of phosphoglycolate, which is a sink for phos-
phorus and an inhibitor of photosynthesis (Falkowski
& Raven, 2007). Hydrolysis of phosphoglycolate pro-
duces inorganic phosphate and glycolate, thereby
reducing the concentration of phosphoglycolate and
recycling valuable phosphorus.
Allelochemicals
Allelopathy was a term first used by Molisch (1937;
cited by Rice, 1979) to describe ‘biochemical interac-
tions between all types of plants including microor-
ganisms’. The consequences of those interactions
could be either beneficial or detrimental to the organ-
isms involved. Allelochemicals, according to the ori-
ginal definition, can have stimulatory effects;
however, the vast majority of work has focused on
the inhibitory effect of allelochemicals (Gross, 2003).
Indeed, Legrand et al. (2003) defined allelochemicals
associated with phytoplankton as secondary metabo-
lites that are released into the surrounding medium
where they act as infochemicals or injurious agents.
They concluded that allelopathic interactions between
phytoplankton are an important aspect of competition.
For example, cell-free filtrate from the prymnesio-
phyte Prymnesium parvum inhibits the growth of the
diatom Thalassiosira weissflogii and the nutrient sta-
tus of the diatom affects its response to the filtrate
(Fistarol et al., 2005). The most common effects of
allelochemicals are cell lysis and growth inhibition
(Legrand et al., 2003). Being defined by function,
allelochemicals have diverse chemical structures and
molecular weights (Leão et al., 2009). Karenia brevis
produces multiple small (500 to 1000 Da) allelochem-
icals containing aromatic groups that inhibit the
growth of the diatom Asterionellopsis glacialis
(Prince et al., 2010). In contrast, the raphidophyte
Heterosigma akashiwo releases a high molecular
weight polysaccharide-protein complex (> 1 000 000
Da) that inhibits the growth of the diatom Skeletonema
costatum by binding to the surface of the cells
(Yamasaki et al., 2009). There is an extensive and
rapidly growing literature on allelopathy associated
with phytoplankton, which is beyond the scope of
D. C. O. Thornton
this review (see reviews by Gross, 2003; Legrand
et al., 2003; Leão et al., 2009).
Resource acquisition
Phytoplankton, like all microorganisms, produce
extracellular proteins in the form of enzymes.
Extracellular enzymes are used by phytoplankton to
acquire inorganic nutrients. Extracellular enzymes
may be closely associated with the cell, such as
located in the periplasmic space, or adhered to the
cell surface. They may also be released into the sur-
rounding medium, where they will contribute to
DOM. Examples of extracellular enzymes produced
by phytoplankton include carbonic anhydrases (CA)
(see reviews by Raven, 1997; Giordano et al., 2005)
and extracellular alkaline phosphatase (AP) (Xu et al.,
2010). Extracellular DOM may play other roles in
resource acquisition. Exopolymers released by micro-
organisms may act to trap exoenzymes in the proxi-
mity of the cell, thereby ensuring that the cell that
released the enzymes benefits most from the resources
created by the enzyme activity (Decho, 1990).
Extracellular saccharides enhance the bioavailability
of iron to eukaryotic phytoplankton in the Southern
Ocean (Hassler et al., 2011). This may be a significant
finding, given that iron is the primary limiting nutrient
over a significant area of the world ocean and carbo-
hydrates are a major component of the DOM released
by phytoplankton.
Autocatalytic cell death
The process of death in phytoplankton has been over-
looked until the last decade. It was generally assumed
that individual phytoplankton cell lines were immortal
unless an external factor (predation, viral infection or
sinking into prolonged darkness) caused their death
(Kirchman, 1999; Bidle & Falkowski, 2004; Franklin
et al., 2006). Recent research has shown that phyto-
plankton also undergo the physiological process of
autocatalytic cell-suicide, which can lead to lysis of
the cells; this process is analogous to programmed cell
death (PCD) in metazoans (Bidle & Falkowski, 2004;
Franklin et al., 2006). Autocatalytic cell death is a
process that is indicated by multiple changes within
the phytoplankton cell and it is often difficult to char-
acterize such cells as clearly dead or alive (Franklin
et al., 2006, 2012). Cell membrane integrity is used as
an early indicator of cell death (Veldhuis et al., 2001).
Veldhuis et al. (2001) showed that a significant pro-
portion of phytoplankton populations grown in cul-
ture and in the field (North Atlantic during March) had
compromised cell membranes, as indicated by
SYTOX Green staining (Fig. 7). Veldhuis et al.
(2001) hypothesized that ‘automortality’ is a signifi-
cant source of DOM leakage, particularly as cells with
compromised cell membranes are often still capable of
32
C
B
A
Fig. 7. Cell permeability in the diatom Thalassiosira weiss-
flogii (CCMP 1051) visualized by epifluorescence microscopy.
Cells were stained with SYTOX Green (Invitrogen, Life
Technologies, Grand Island, U.S.A.), a membrane-imperme-
able nucleic acid stain. Chlorophyll autofluorescence is shown
in red and SYTOX Green stained nucleic acids are shown in
green. A. Intact cell containing chlorophyll but no SYTOX
Green staining and therefore intact cell membranes. B. Intact
cell containing chlorophyll with compromised cell membranes
revealed by the staining of an intact nucleus with SYTOX
Green. C. Dying cell with low chlorophyll autofluorescence,
a disrupted nucleus and compromised cell membranes. Image
courtesy of Jie Chen. Scale bar = 10 µm.
photosynthesis. Subsequent work has shown that
stresses such as low irradiance or nutrient limitation
affect compromised plasma membranes and autocata-
lytic cell death in phytoplankton (Berman-Frank et al.,
2007; Timmermans et al., 2007; Franklin et al., 2012).
DOM release and microbial food webs
In the ‘classic food web’ organic carbon fixed by
photosynthesis is passed as POM from phytoplankton
to herbivorous grazers and then to fish, whereas the
microbial loop is driven by DOM (Azam et al., 1983;
Ducklow, 1983). The release of DOM by phytoplank-
ton is a significant driver of secondary production by
heterotrophic prokaryotes. Generally, DOM release
by phytoplankton is considered insufficient to support
the observed heterotrophic bacterial growth (Baines &
Pace, 1991; Nagata, 2000; Morán et al., 2002b; Teira
et al., 2003b). In addition, processes such as viral lysis
and sloppy feeding contribute a significant amount of
the phytoplankton DOM that is utilized by bacteria.
Baines & Pace (1991) concluded that the DOC
released by phytoplankton supports less than 50% of
bacterial carbon requirements, based on a review of
data from freshwater, estuarine and coastal environ-
ments, and modelling. Recent work has challenged
this general assumption: DOC released by
Phytoplankton DOM release
phytoplankton is sufficient to support the observed
bacterial growth in the Southern Ocean (Morán
et al., 2001, 2002b; Morán & Estrada, 2002) and in
an area of coastal upwelling off the Iberian Peninsula
in the Atlantic (Teira et al., 2003b).
Bacterial growth efficiency (BGE) is a key factor in
determining whether sufficient DOC is released from
phytoplankton to support bacterial growth. BGE is
simply the proportion of the total bacterial carbon
demand that is used for bacterial production:
BGE ¼ BP=ðBP þ BRÞ (2)
where BP is bacterial production and BR is bacterial
respiration (Robinson, 2008). BGE depends on a
number of factors, including DOM composition and
composition of the microbial community. The median
value of BGE in the coastal ocean is 0.16 (0.19 ± 0.16;
mean ± SD) compared with 0.08 (0.14 ± 0.14) in the
open ocean (Robinson, 2008). Therefore, although
PER in oligotrophic waters is relatively high, the
DOC released by phytoplankton is generally insuffi-
cient to support bacterial growth (Teira et al., 2003b;
López-Sandoval, 2011). This is probably because the
nutrient limitation that drives the photosynthetic over-
flow of organic carbon into the DOC pool also limits
the ability of bacteria to utilize the DOC pool.
The interactions between heterotrophic prokar-
yotes and phytoplankton are poorly understood. An
early concept used to describe the relationship
between phytoplankton and bacterioplankton was
the ‘phycosphere’ (Bell & Mitchell, 1972; Stocker,
2012), which described a zone surrounding a phyto-
plankton cell in which bacterial growth is stimulated
by DOM released from the cell. Bell et al. (1974)
grew two strains of bacteria with the diatom
Skeletonema costatum and found that the growth of
one bacterial strain was stimulated by the presence of
the diatom while the growth of the second was inhib-
ited. They concluded that the release of DOM by
phytoplankton is important in determining bacterial
community structure. Modern culture-independent
molecular methods enable detailed investigations of
the bacteria associated with phytoplankton. For
example, there was a succession of bacterial species
attached to cells of the dinoflagellate Lingulodinium
polyedrum during a bloom off the Californian coast
(Mayali et al., 2011).
Interactions between bacteria and phytoplankton
may be both ‘top down’ and ‘bottom up’ at the same
time. While the composition of the DOM released by
phytoplankton may affect the growth and community
structure of the bacterial community (Sapp et al.,
2007; Pete et al., 2010), the bacteria will also affect
the amount and composition of DOM released by the
phytoplankton (Bruckner et al., 2011; Gärdes et al.,
2011, 2012). Marinobacter adhaerens was isolated
from marine particles in the German Wadden Sea and
33
its complete genome sequenced (Gärdes et al.,
2010). Subsequently, it has been grown with the
diatom Thalassiosira weissflogii in a model system
(Gärdes et al., 2012) in experiments showing that the
interaction between the diatom and the bacterium
depend on the nutrient status of the culture. Under
‘balanced’ nutrient conditions (N : P of 16 : 1), the
bacterium enhanced exudation and TEP formation in
batch cultures compared with axenic controls.
However, if the cultures were grown under condi-
tions resulting in nutrient limitation, M. adhaerens
did not enhance TEP production. Aggregate forma-
tion is an important process, as it changes the size
distribution of particles in the water column and
affects the efficiency of the biological carbon pump,
because larger particles sink faster than small parti-
cles. Diatoms, particularly under nutrient-limiting
conditions, exude sticky polymers (such as TEP pre-
cursors) that affect aggregation (Thornton, 2002).
Gärdes et al. (2011) showed that bacteria are impor-
tant in the aggregation of Thalassiosira weissflogii;
aggregation did not occur in axenic cultures of the
diatom, whereas bacteria attached to T. weissflogii
cells enhanced aggregation.
The interactions between phytoplankton and het-
erotrophic prokaryotes that affect DOM release by
phytoplankton are complex and largely unpredictable
with our current knowledge. Bacterial community
composition affects the composition of the phyto-
plankton community and vice versa. Environmental
factors, such as nutrient limitation, moderate these
interactions by affecting the physiology of the organ-
isms and their allocation of resources. Consequently,
the concentration and amount of DOM released by
phytoplankton in natural waters are an emergent prop-
erties of the interactions between organisms and the
surrounding environment.
Phytoplankton DOM release and global climate
change
A major research challenge over the coming decades
will be to evaluate the impact of global climate change
on ecosystems and the ecosystem services that sustain
human populations. The carbon dioxide mixing ratio
in the atmosphere has risen from a pre-industrial value
of 280 ppm (Caldeira & Wickett, 2003) to a current
value of 394 ppm as measured at the Mauna Loa
Observatory, Hawaii (NOAA, October 2013 value).
The increasing amount of CO2 in the atmosphere is
both trapping more heat in the troposphere and sig-
nificantly altering the carbonate chemistry of the
upper ocean. These changes have resulted in a mean
warming of the Earth’s surface by 0.85°C over the
period from 1880 to 2012 (IPCC, 2013) and a
decrease in the pH of the surface ocean from a pre-
industrial value of 8.2 to approximately 8.1 today
(Royal Society, 2005). Key questions are: How will
D. C. O. Thornton
a warmer and more acidic ocean affect the structure
and function of marine ecosystems? Will the ability of
these altered ecosystems to sequester carbon change,
and how will this feedback to the amount of carbon
dioxide in the atmosphere?
Processes affecting the partitioning of organic car-
bon between the dissolved and particulate phases will
play a significant role in determining the fate of carbon
in the ocean as the climate changes. It is predicted that,
as the Earth warms, the surface ocean will become
both warmer and more stratified (Sarmiento et al.,
2004; Behrenfeld et al., 2006). An increasingly stra-
tified surface ocean will be increasingly nutrient lim-
ited, as there will be less mixing between the nutrient-
depleted surface waters and the nutrient-rich deep
waters. Thus, the photic zone will support a lower
biomass of primary producers. In addition, the pH of
the surface ocean will continue to decline, with a pH
of 7.9 predicted for the end of the century and 7.4
predicted for the end of the millennium (Caldeira &
Wickett, 2003). Potentially, therefore, phytoplankton
living in large areas of the future ocean will be grow-
ing in an environment that is warmer than today, with
a lower pH and lower availability of inorganic nutri-
ents. These predicted changes will result in a more
stressful environment for phytoplankton growth and,
as already discussed, stresses such as high temperature
and nutrient limitation affect DOM release by phyto-
plankton. Moreover, conditions of increased stratifica-
tion and nutrient limitation would be expected to
favour small-celled taxa (Finkel et al., 2010) with
relatively large surface area to volume ratios and
therefore greater potential for DOM loss via leakage.
Successful integration of processes that occur over a
range of temporal and spatial scales, from the physiol-
ogy of individual phytoplankton cells to ocean circu-
lation, is required to meet the challenge of
understanding the effect of climate change on carbon
cycling in the ocean. Over the next few paragraphs I
will explore the evidence to support the hypothesis
that phytoplankton PER will be greater as a result of
climate change induced by increasing CO2 in the
atmosphere.
Temperature and stratification
There is convincing evidence that the upper ocean is
becoming warmer (Levitus et al., 2000; Barnett et al.,
2005; Lyman et al., 2010). Environmental tempera-
ture has a profound effect on the physiology of phy-
toplankton metabolism and there are several reviews
that address these effects in relation to climate change
(Beardall & Raven, 2004; Finkel et al., 2010; Winder
& Sommer, 2012). However, the effect of temperature
on DOM release has generally been overlooked.
Diatoms become more ‘sticky’ at elevated tempera-
tures and prone to forming aggregates (Thornton &
Thake, 1998; Piontek et al., 2009; Rzadkowolski &
34
Thornton, 2012), which may be affected by the
enhanced release of DOM by phytoplankton at ele-
vated temperatures. Aggregate formation at elevated
temperature has been hypothesized to be due to sticky
polymers on the surface of the diatoms (Thornton &
Thake, 1998) or the production of TEP (Piontek et al.,
2009). Seven of eight phytoplankton species studied
by Claquin et al. (2008) produced more TEP with
increasing temperature when grown in batch culture.
The trend continued until a maximum TEP production
rate was reached, with higher temperatures resulting
in lower TEP production rates. The exception to this
trend was the prymnesiophyte Emiliana huxleyi,
which showed no relationship between TEP produc-
tion rate and temperature. There is evidence from
mesocosm experiments for increased DOM release
by natural phytoplankton grown at elevated tempera-
ture (Engel et al., 2011; Wohlers et al., 2009). The C :
N ratio of the DOM increased at a higher temperature
due to increased production of dissolved carbohy-
drates (Engel et al., 2011). Short-term (6 h) warming
experiments with natural phytoplankton communities
from the Southern Ocean showed that increasing tem-
perature from ambient (−1.4 to 0.4°C) to 2°C resulted
in an increase in PER from 35 to 54% (Morán et al.,
2006). While PPP remained relatively constant (0.7
mg C m−3 h−1), there was an increase in DPP from 0.5
to 0.9 mg C m−3 h−1 (Morán et al., 2006).
An increase in PER with climate change may not
result in an increase in the total amount of DOM
released by phytoplankton if the ocean supports a
lower phytoplankton biomass. Long-term field data-
sets with sufficient coverage and resolution to enable
scientists to determine whether global warming affects
changes in phytoplankton distribution and abundance
are lacking. Boyce et al. (2010a) concluded that glo-
bal phytoplankton concentration is declining rapidly
in the ocean at a rate of approximately 1% year−1 in
response to warming temperatures, using pigment and
Secchi depth data going back to 1899. However, this
conclusion was immediately challenged by several
groups (Mackas, 2010; McQuatters-Gollop et al.,
2010; Rykaczewski & Dunne, 2010). More work has
been done at the regional scale. In the North Sea and
North Atlantic, the Continuous Plankton Recorder
(CPR) survey has produced data since 1931 on the
distribution of larger phytoplankton (Leterme et al.,
2005). CPR data is generally collected from latitudes
higher than 40° N and is biased towards shelf waters
(Boyce et al., 2010b). The plankton colour index
(PCI), a crude estimate of phytoplankton biomass,
has increased since 1958, with a decline in the relative
abundance of diatoms compared with dinoflagellates
(Leterme et al., 2005). Based on satellite-derived
ocean colour data, the area of waters with the lowest
chlorophyll concentrations (< 0.07 mg chl m−3) asso-
ciated with the subtropical gyres (waters from 5° N to
45° N, and 5° S to 45° S) has expanded globally by 6.6
Phytoplankton DOM release
million km2, or 15%, from 1998 through to 2006
(Polovina et al., 2008). The expansion correlated
with an increase in mean monthly sea surface tem-
perature and was hypothesized to be the result of
increased stratification causing an expansion of oligo-
trophic waters. Modelling studies have also shown an
expansion of the subtropical gyres and increased stra-
tification of the ocean since the industrial revolution,
in response to warming of the surface ocean
(Sarmiento et al., 2004; Bopp et al., 2005).
Behrenfeld et al. (2006) used satellite-derived ocean
colour data to relate the annual productivity of the
ocean to climate variability. Annual global productiv-
ity was low in years in which there was enhanced
stratification, as this resulted in a larger area of low
latitude, low productivity waters. Phytoplankton pro-
ductivity is predicted to increase at high latitudes in a
warmer ocean due to an extended growing season
caused by reduced mixing; however, this will be
insufficient to balance the reduction observed at
lower latitudes (Bopp et al., 2005; Doney, 2006).
These examples illustrate that the effect of global
warming on phytoplankton biomass is regional and
there is currently no robust global integration of these
observations (Polovina et al., 2008). Lower biomass
would be predicted to result in a lower release of DOM
if the phytoplankton community does not change.
However, it is unlikely to be this simple as the changes
that affect phytoplankton biomass also affect commu-
nity composition.
Coupled climate and biogeochemical models indi-
cate that the biomass of diatoms will decrease with
predicted climate change, relative to small phyto-
plankton, as a result of increased stratification and
consequent decreased nutrient supply to surface
waters at mid latitudes (Bopp et al., 2005; Marinov
et al., 2010). The prediction of smaller cells in a
warmer ocean is also supported by the geological
record (Falkowski & Oliver, 2007). Falkowski &
Oliver (2007) hypothesized that the negative correla-
tion between the surface area of diatom frustules and
ocean temperature over the last 65 million years was
not a direct function of temperature, but rather the
result of lower nutrient supply to the surface ocean
caused by reduced vertical mixing in warmer oceans.
Similarly, resource availability is key to explaining the
success of different algal size classes at different tem-
peratures in the contemporary ocean (Marañón et al.,
2012). Data from the Atlantic Ocean show water
temperature affects phytoplankton cell size, with pico-
phytoplankton becoming more dominant at warmer
temperatures (Morán et al., 2010). Communities
dominated by picophytoplankton in the Atlantic
Ocean have higher PER than phytoplankton commu-
nities dominated by larger cells (Teira et al., 2001a,
2001b). However, in the field it is difficult to uncouple
nutrient limitation and temperature effects. In the
laboratory, Montagnes & Franklin (2001) grew five
35
species of diatom and two flagellates and found that
growth rate increased with temperature, but cell
volume decreased at a rate of 4% °C−1. A meta-ana-
lysis of the literature also found that protists decreased
in cell volume with temperature at a similar rate (2.5%
°C−1; Atkinson et al., 2003). Results from short-term
laboratory experiments, during which natural phyto-
plankton communities from the Baltic Sea were
exposed to varying degrees of nutrient stress at differ-
ent temperatures, support the hypothesis that nutrient
limitation mediates temperature effects on cell size
(Peter & Sommer, 2013).
Ocean acidification
The dissolved inorganic carbon (DIC) concentration
of seawater is approximately 2000 µM (Falkowski &
Raven, 1997; Morel et al., 2002); however, the con-
centration of dissolved CO2 is only 10–20 µM
(Falkowski & Raven, 1997; Morel et al., 2002). This
value is below the half saturation constant of 30–40
µM for diatom RuBisCO (Badger et al., 1998; Morel
et al., 2002), which suggests that phytoplankton
photosynthesis could be CO2-limited in the contem-
porary ocean. Culture work has shown that the growth
rate of diatoms is limited by CO2 supply under optimal
conditions of light and nutrients (Riebesell et al.,
1993). Increasing concentrations of carbon dioxide
in the atmosphere will result not only in higher DIC
concentrations in the surface ocean, but also in a shift
in the equilibrium of the different components of the
DIC systems as the ocean acidifies, resulting in higher
dissolved CO2 concentrations (Royal Society, 2005).
Carbon fixation rates may increase if more CO2 is
available, resulting in photosynthetic overflow if the
increased availability of organic carbon is not matched
by an increased availability of other nutrients within
the phytoplankton cell. There is evidence that elevated
dissolved CO2 concentrations facilitate photosynth-
esis and affect the release of DOM by phytoplankton
(Riebesell, 2004). However, phytoplankton response
to increasing dissolved CO2 concentrations is unlikely
to be straightforward as most have carbon concentrat-
ing mechanisms (Giordano et al., 2005) and, there-
fore, are not limited by the current concentration of
dissolved CO2 in seawater. Consequently, photo-
synthesis may not be significantly stimulated under
ocean acidification conditions (Beardall & Raven,
2004; Royal Society, 2005) and there may be shifts
in phytoplankton community structure as the ocean
acidifies based on the competitive costs and benefits of
different inorganic carbon acquisition strategies.
Low pH may affect the rate of processes transform-
ing DOM, such as the formation of exopolymer parti-
cles from dissolved precursors and the enzymatic
hydrolysis of organic matter in the ocean. Research
has shown increased abiotic TEP formation with
decreasing pH (Mari, 2008) and increased production
D. C. O. Thornton
of extracellular carbohydrates by a diatom with
decreasing pH (Thornton, 2009). However, as pointed
out by Passow (2012), the work of Mari (2008) and
Thornton (2009) is not representative of the future
ocean, as both researchers added acid to titrate the
seawater to a lower pH under current atmospheric
CO2 mixing ratios, resulting in a change in total alka-
linity. In the future ocean the low pH will be asso-
ciated with higher DIC concentrations, but no change
in total alkalinity (Passow, 2012). Passow (2012)
showed that the abiotic formation of TEP from pre-
cursors is not affected by ocean acidification. These
examples illustrate that many of the apparent discre-
pancies between results from ocean acidification
experiments arise from the experimental design.
The degradation of phytoplankton-derived DOM in
the future ocean will depend on complex interactions
between microorganisms as ocean acidification will
affect the composition and concentration of the DOM
produced by individual taxa, the composition of the
microbial community and potentially the chemistry of
extracellular enzymes (Arnosti et al., 2011). The com-
plexity of these relationships is shown by recent
research. For example, extracellular glucosidase activ-
ity was enhanced under conditions simulating ocean
acidification, leading to a greater degradation of algal-
derived polysaccharides (Piontek et al., 2010). Other
work has found that acidification had negligible
effects on some enzymes and reduces the activity of
others (Yamada & Suzumura, 2010).
Several experiments have been conducted in which
natural populations of phytoplankton were grown in
experimental systems with elevated atmospheric car-
bon dioxide mixing ratios to simulate future climate
change scenarios. Kim et al. (2011) grew natural
populations of microorganisms from Korean coastal
waters under control (ambient) conditions, acidifica-
tion (900 ppm CO2), and acidification with warming
(3°C warmer than ambient), in 3000 l mesocosms. At
the end of the batch experiment, during nitrogen
depletion, DOC concentrations were lowest in the
control treatment and highest in the acidification-
with-warming treatment. The ratio of DOC to POC
was lowest in the control and highest in the acidifica-
tion-with-warming treatment. This suggests that PER
was greater than the control under conditions of acid-
ification, and greatest under conditions of acidification
with warming. However, Kim et al. (2011) did not
measure the photosynthetic allocation of carbon into
PPP and DPP and therefore their measurements are
not equivalent to PER. Riebesell et al. (2007) con-
ducted mesocosm experiments with natural phyto-
plankton assemblages grown under atmospheres
containing three different CO2 mixing ratios (350,
700 and 1050 ppm) and found that the drawdown of
DIC increased with increasing DIC concentrations,
though the drawdown of other nutrients was not
enhanced. There was an increase in the loss of organic
36
carbon from the upper mixed layers of the mesocosms
grown under acidified conditions. Riebesell et al.
speculated that TEP may have played a significant
role in the transformation of DOC to POC and the
sinking of POC from the upper layer of the meso-
cosms with high pCO2. However, analysis of the
TEP concentrations from the same experiment by
Egge et al. (2009) showed no difference in TEP pro-
duction between the different pCO2 treatments.
Recently, experiments using mesocosms in Arctic
waters showed enhanced production of DOC by phy-
toplankton grown under elevated CO2 (Engel et al.,
2013).
Future research
DOM release by phytoplankton has been a subject of
research for more than 50 years. Despite this sustained
interest, there remain many unresolved questions
regarding the physiological processes that affect
DOM release by marine phytoplankton and its bio-
geochemical significance. Many of our current expla-
nations for DOM release are hypotheses that require
further testing. Fortunately, new instrumentation for
analytical geochemistry, the ‘omics’ methods of biol-
ogy, and the data handling tools of bioinformatics will
make it feasible to open the ‘black box’ of DOM
biogeochemistry over the next few decades. In the
following section, I will highlight some of the gaps
in our current knowledge and suggest how future
research can fill those gaps.
Physiology of phytoplankton DOM release
The physiological status of the cell affects both the
amount and composition of the DOM released into the
surrounding medium. Flynn et al. (2008) considered a
lack of understanding of DOM release by phytoplank-
ton to be a significant gap in our knowledge of phy-
toplankton physiology and a limitation for current
biogeochemical models of primary production. If exu-
dation is an active process, then presumably it is of
some benefit to the phytoplankton. In some examples,
such as extracellular enzymes, it is easy to envision
the potential return on the investment of synthesizing
the DOM and transporting it across the cell membrane
into the external environment. However, with other
processes, such as photosynthetic overflow, the costs
and benefits are harder to discern. If exudation of
carbohydrates in the stationary phase is really photo-
synthetic overflow when growth is limited, then why
is it often exuded in the form of complex heteropoly-
mers (high molecular weight [HMW] DOM) rather
than low molecular weight (LMW) DOM? For exam-
ple, the mean proportion of HMW (> 12 000 Da)
carbohydrates produced by Skeletonema costatum
increased from 20 ± 11% (mean ± SD) in the expo-
nential phase to 72 ± 18% in the stationary phase
Phytoplankton DOM release
(Malej & Harris, 1993). Complex heteropolymers
should have a relatively high cost to synthesize and
transport out of the cell, in contrast to, say, glucose,
which is a direct product of photosynthesis and more
likely to diffuse out of the cell. Photosynthetic over-
flow is invoked as a mechanism for coping with
excess fixed carbon during nutrient limitation.
However, the cellular machinery (RNA, proteins and
vesicles) necessary for the synthesis of polymers
requires likely limiting nutrients (e.g. N and P).
These inconsistencies suggest that photosynthetic
overflow is more complex than we currently appreci-
ate, or that photosynthetic overflow is not the reason
for this form of exudation.
Little is known of the physiology of DOM release
by eukaryotic phytoplankton and there is a need for
more research on the intracellular assembly, transport
and subsequent extracellular release of DOM by phy-
toplankton. The term ‘exudation’ is poorly defined,
reflecting our limited understanding of the physiolo-
gical mechanisms affecting the release of DOM by
phytoplankton (Chin et al., 2004). The secretion of
polymers via exocytosis was observed in the prymne-
siophyte Phaeocystis globosa, which is known to
produce copious amounts of polymeric gels (Chin
et al., 2004). The secretory vesicles inside cells of
P. antarctica were shown to contain DMSP and
DMS in addition to polymers (Orellana et al. (2011),
suggesting that these small molecules may also be
secreted via exocytosis. The relative contributions of
exudation and leakage to DOM release, and how the
physiological status of the cells affects them, remain
to be determined. Novel methods will be required to
distinguish between the DOM released by passive
leakage across the cell membrane and the DOM that
is actively exuded.
The ecological significance of autocatalytic cell
death of phytoplankton is unknown and there is
much to be learnt about the physiology of the process
(Bidle & Falkowski, 2004, Franklin et al., 2006). It is
well established that cell membranes become more
‘leaky’ during cell death (Fig. 7; Veldhuis et al.,
2001), but how much DOM this produces is unknown.
It may be that the few dying cells in a population
determine the amount and composition of the DOM
released, as they have such high rates of leakage
compared with the general population. There is a
need to investigate the effect of phytoplankton cell
death on the partitioning of the organic matter released
between the dissolved and particulate pools. Factors
affecting the permeability of phytoplankton cell mem-
branes and the subsequent leakage of organic matter
from the cells are largely unknown. Stress is predicted
to make cell membranes more leaky, but there is little
information on how stress affects the composition and
amount of DOM passing through the cell membrane,
or how the cell membrane itself changes. It may be
that different stresses affect DOM production in
37
different ways. For example, does P limitation limit
the ability of phytoplankton to repair their cell mem-
branes, resulting in significant leakage? Dyhrman
et al. (2012) showed that Thalassiosira pseudonana
changes the composition of its lipids in response to P
limitation, though they did not investigate whether
these changes affected DOM release by the diatom.
Rhythms of phytoplankton activity in response to
the light–dark cycle and other stimuli may affect the
balance between exudation and leakage and the com-
position of the DOM released. Such effects have lar-
gely been overlooked, though it is well established
that EPS production by benthic diatoms is affected by
light–dark cycles (Staats et al., 2000; Smith &
Underwood, 2000). Crocosphaera watsonii, an eco-
logically significant N-fixing cyanobacterium, has
diel cycles of carbohydrate accumulation and release,
with the internal carbohydrate pool decreasing as the
cells release EPS and TEP into the surrounding water
(Dron et al., 2012).
Finally, the new ‘omic’ approaches have great
potential to contribute significantly to understanding
the physiology of DOM release by phytoplankton.
The draft genomes of several important phytoplank-
ton species have been published over the last decade
(Rynearson & Palenik, 2011). Publication of the anno-
tated genomes of the diatoms Thalassiosira pseudo-
nana (Armbrust et al., 2004) and Phaeodactylum
tricornutum (Bowler et al., 2008) produced a vast
amount of data on the potential physiology of these
organisms, including information on nutrient trans-
port and metabolic pathways. A new understanding
of the diatom genome has led to research on gene
expression in stressed diatoms using transcriptomic
and proteomic approaches. For example, recent work
with T. pseudonana has shown that it has a sophisti-
cated suite of biochemical strategies to deal with
phosphorus deficiency (Dyhrman et al., 2012) and
putative death-related genes play a role in acclimation
to low iron conditions (Thamatrakoln et al., 2012).
Similar approaches could be used to investigate gene
expression associated with metabolic pathways and
transport proteins associated with exudation and leak-
age. Genomics provides information on which genes
are present in an organism and transcriptomics tells us
under what conditions those genes are expressed.
However, neither of these approaches tells us anything
about rates of processes. Consequently, ‘omic’
approaches should be used in conjunction with tradi-
tional physiological measurements of rates for the
greatest insight into DOM release.
Chemical characterization of DOM released by
phytoplankton
The chemical characterization of marine DOM is an
on-going challenge for geochemists (Kujawinski,
2011). It is sobering to consider that even measuring
D. C. O. Thornton
the concentration of DOC in seawater, let alone its
composition, was a challenge until the 1990s (Sharp,
2002). Marine DOM is basically treated as a ‘black
box’ in biogeochemical models or crudely character-
ized by molecule size (LMW or HMW) or reactivity
(labile or refractory) (Christian & Anderson, 2002).
Better characterization of the DOM released by phy-
toplankton will contribute to continuing efforts to
understand the composition of marine DOM in rela-
tion to its sources, reactivity, transformations and
sinks. The complexity and chemical diversity of
DOM mean that opening the ‘black box’ of DOM
composition will remain a significant challenge over
the coming decades. However, new analytical tools
are being developed that may provide significant
insights into this problem. For example, electrospray
ionization coupled to mass spectrometry is being used
to explore the composition of the largely uncharacter-
ized LMW fraction of DOM (Kujawinski, 2011).
HMW DOM has been better characterized than
LMW DOM (< 1000 Da), even though small mole-
cules make up the bulk (approximately 70%) of the
DOM pool (Kujawinski, 2011). Characterization of
the composition of LMW DOM, both in phytoplank-
ton cultures and in situ, is the first step in determining
its sources and biogeochemical significance. At the
other end of the size spectrum, the HMW DOM that
contributes to exopolymer particles has been poorly
characterized. It is likely that both TEP and CSP
contain chemical components other than those that
stain with the dyes that define them (Figs 2–5). TEP
plays an important role in the biogeochemistry of the
biological carbon pump (Passow & Carlson, 2012)
and consequently there is a need to better define its
composition to determine its origin and biogeochem-
ical significance. Much of the recent detailed work on
the composition of EPS produced by diatoms has been
conducted with laboratory-grown cultures of benthic
epipelic diatoms (Underwood et al., 2004; Bellinger
et al., 2005; Abdullahi et al., 2006). There is no reason
why the techniques used in this research could not be
applied to ecologically relevant taxa of
phytoplankton.
Climate change and phytoplankton DOM release
Determining how phytoplankton will respond to a
warming and acidifying ocean is going to be a key
research theme over the coming years. While much
progress has been made, there are as yet too many
unknowns to enable scientists to make reliable predic-
tions on how phytoplankton will respond to climate
change. Understanding phytoplankton DOM release
is one component of this significant problem.
Creating experimental conditions that realistically
simulate ocean acidification remains a challenge (Rost
et al., 2008; Hurd et al., 2009). Acidification is gen-
erally achieved by titrating the culture to the desired
38
pH (using HCl and NaOH) or by bubbling the system
with air containing an elevated mixing ratio of CO2
(Rost et al., 2008; Hurd et al., 2009). Manipulating the
pH and DIC system in seawater is complex, as CO2
both dissolves in and reacts with seawater (Dring,
1982). Furthermore, phytoplankton physiology
affects the pH of seawater, as photosynthesis increases
pH and respiration decreases it. Koeve & Oschlies
(2012) suggested that DOM release by phytoplankton
(e.g. organic acids) may be a further source of error in
the characterization of the DIC system during acidifi-
cation experiments. These effects are pronounced in
phytoplankton cultures where cell concentrations are
generally high. Poor control and characterization of
the DIC system during culture experiments may
explain some of the inconsistencies in experiments
conducted with single species, such as Emiliania hux-
leyi (Hurd et al., 2009; Hoppe et al., 2011). Flynn
et al. (2012), in a recent modelling study, showed that
the pH and DIC system may be significantly different
at the cell surface than in the bulk medium. This
difference will become more pronounced as the
ocean acidifies and the buffering capacity of the
ocean is reduced. Differences were greatest between
the surface of the cell and the bulk medium in cells
that were large with a greater metabolic activity. These
results suggest that research considering the effects of
climate change on phytoplankton permeability and
DOM release should consider the microenvironment
immediately surrounding the cell in addition to the
bulk medium. Collectively, these results suggest that
researchers need to pay more attention to the design of
ocean acidification experiments with phytoplankton
cultures, in terms of how to control conditions within
the experiments and accurately monitor DIC (Rost
et al., 2008; Hurd et al., 2009; Hoppe et al., 2012).
Most experiments investigating the effect of cli-
mate change have been relatively short term.
Laboratory grown cultures are generally acclimated
to experimental conditions for 7–10 generations
before the experiment begins and the experiment is
completed within a few days or weeks (Hurd et al.,
2009). These experiments show how individuals
change their patterns of gene expression, but the
genetic composition of the population does not sig-
nificantly change over the course of the experiment
(Collins, 2012). The ocean is warming and acidifying
rapidly; nonetheless, significant climate change in the
surface ocean will encompass a time span of thou-
sands to tens of thousands of generations of phyto-
plankton and so phytoplankton will be evolving as
well as acclimating in response to the observed rate of
ocean change. Microevolution may be occurring
through the selection of particular clones or genotypes
within a species and from de novo mutations (Collins,
2012). Researchers have started to investigate the
evolutionary adaptation of phytoplankton to climate
change and indeed, phytoplankton make good model
Phytoplankton DOM release
organisms for investigating evolution in eukaryotes,
as they are small and have generation times of one or
two days. Significant phenotypic changes in some
strains of the freshwater green alga Chlamydomonas
occurred when they were grown under elevated CO2
for more than 1000 generations (Collins & Bell,
2004). Lohbeck et al. (2012) conducted evolution
experiments that lasted at least 500 generations with
Emiliania huxleyi grown under control and elevated
CO2 conditions. When both control and elevated-CO2
strains were grown under ocean acidification condi-
tions, the elevated-CO2 strains were better adapted to
acidified conditions, as they had faster growth rates
and were able to calcify better than the controls. In
contrast, there was little evidence of adaptation after
100 generations in the diatom Thalassiosira pseudo-
nana grown under CO2 and pH predicted for the end
of the century, compared with contemporary condi-
tions (Crawfurd et al., 2011). Temperature has also
been used as a selection pressure in phytoplankton
growth experiments, with significant adaptation to
elevated temperature observed over multiple genera-
tions (Huertas et al., 2011). Similar experiments could
be conducted to determine how the amount and com-
position of DOM released from different phytoplank-
ton taxa will change as they adapt in response to the
selection pressure of climate change.
Perhaps the greatest challenge to determine the
effect of climate change on DOM release by phyto-
plankton is accounting for interactions between dif-
ferent abiotic and biotic components of marine
ecosystems (Rost et al., 2008). Much of the work
that has been carried out so far has looked at either
warming or acidification in isolation, whereas in rea-
lity the ocean’s pH is decreasing as it warms. Gao
et al. (2012) found that high CO2 and high light
interact synergistically to reduce the primary produc-
tivity of natural assemblages in the South China Sea.
Interactions between organisms also affect the com-
position and amount of DOM produced by phyto-
plankton (Gärdes et al., 2011, 2012). The
complexity of this challenge is illustrated by the evo-
lution experiments discussed above: in situ selection
pressures will be a product of warming, elevated CO2
and the resulting interactions between organisms. To
date, evolution experiments have used acidification or
warming as a selection pressure in isolation, as it is too
complex to set up manageable experiments account-
ing for interactions. A good place to start to examine
this complexity would be to determine the effect of
both warming and acidification on phytoplankton
growth and DOM release in simple laboratory mono-
culture experiments.
There is now sufficient work on the effect of climate
change on phytoplankton ecology to enable some
broad generalizations that can be used to generate
hypotheses for future work. Overall, the future ocean
will be warmer, more acidic and more stratified than it
39
is at present. Increased stratification will result in a
lower supply of nutrients to the photic zone. These
stresses (elevated temperature, acidification, high
light and low nutrients) all cause phytoplankton to
release more DOM into the surrounding water,
through a combination of processes associated with
leakage and exudation (Fig. 6). In addition, low nutri-
ent, stratified conditions will select for small phyto-
plankton, which tend to leak a greater proportion of
their organic carbon to the surrounding water.
Therefore, I hypothesize that a greater proportion of
total phytoplankton primary production will be
released into the surrounding water as DOM as the
surface ocean warms and becomes more acidic. This
will have implications for the entire marine carbon
cycle: potentially less organic matter will be available
for metazoan grazers and their predators, more organic
matter will pass through microbial food webs, and the
efficiency of the biological carbon pump will be
reduced, as less POC will be exported from the eupho-
tic and mesopelagic zones into the deep ocean.
Acknowledgements
This research was supported by the National Science
Foundation (U.S.A.) under Grant No. OCE 0726369
from the Division of Ocean Sciences. Any opinions,
findings and conclusions or recommendations expressed
in this material are those of the author and do not neces-
sarily reflect the views of the National Science
Foundation. The author would like to thank two anon-
ymous reviewers, Julie M. Rose and the students who
helped him develop his ideas (particularly Jie Chen and
Michael Pohlen, who generously shared their data).
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