Phvtol.

(1988), UO, 441 461

Temperature and algal growth

BY JOHN A. RAVEN' .^ND RICHARD J. GEIDER-*

^ Department of Biological Sciences, University of Dundee, Dundee DDl 4HN, UK
-Department of Plant Biology, University of Birmingham, P.O. Box 363,
Birmingham B15 2TT, UK
{Received 16 May 1988; accepted 10 July 1988)

C O N T H N T .S
Summary 441 I\". lixphmation ol the effects of tetiiperatiire
I. Introduction 442 o?i resource-satmated algal growth 447
I I . T h e efTects of t e m p e r a t u r e on chemical V. T h e obserxed efTects of t e m p e r a t u r e on
transformations and on transport processes, resource-limited algal growth 452
and possible mechanisms of ameliorating 1. Light limitation 452
their efTects on algae at low temperatures 442 2, Limitation by chetiiical resomces 454
1. T e m p e r a t u r e eflect on cataUsed and \"L Explanation of the efTects of t e m p e r a t u r e
uncataiysed chemical transformation and on resource-limited algal growth 454
transport processes 442 1. Light limitation 454
2, M e c h a n i s m s whereby t h e cell can 2. Limitation by chemical resources 455
ameliorate tlie elfects ol low \ ' l l . Conclusions 45(S
tetiiperatures 445 .AcknowTetlgetnetits 45S
I I I . T h e o b s e r \ e d efTects of t e m p e r a t u r e oti References 45S
resource-saturated algal growth 446

S U M M h R \-
G e n o t y p i c variation in the temperature o p t i m u m lor resource-saturated growth of tiiicroalgae has beeti used to
p r o v i d e envelopes of//,,, ( m a x i m u m specific growlh rate) as a funcfioti of t e m p e r a t u r e . T h e C*,,, \ a l u e for //, for
batch.-cuhured algae with optimal growth t e m p e r a t u r e s in the ratige 5-40 C' is lScS; rather higher values (O,,, =
2 0 8 - 2 1 9 ) are found, albeit with lower /i \'alues at a gi\'en temperature, for continuous ctiltures. T h e envelope
a p p r o a c h selects/;,,, values for the smallest cells from the taxa (metnbers of the Chlorophyta and Bacillariojihyta)
w i t h the highest //,,, \'alues at a g i \ e n tem|ieralure. Larger cell size, or m e m b e r s h i p of the Dinophyta, gives a
decreased /;, at a g i \ e n tetnperature. Fhenotypie change in //, within a g i \ e n genotype grown at sub-optimal
t e m p e r a t u r e s , has a P,,, in exeess ot 188. .'\nalysis of cotistraints on the resource-saturated \ a l u e of// iti the fastest-
throwing micro-algae suggest that, at their temperattire optima, the cells are close (within a factor of 2) to their
m a x i m u m potential growth rate, basetl on the known kinetic properties of their eatalysts, the need for kinetic
h e t e r o g e n i t y in catalyses m metabolie pathways, and the need to allocate some cell resources to structural atid
storage compotients. I'henotypic and genotypic responses to lower t e m p e r a t u r e s for growth, in terms of
reallocation of resources to increase the t|tiantity per unit biomass of c a t a h s t s as a means of offsetting lower
catalytic capacity at lower temperatures, are limited. An exception is the light-har\ esting and reaction centre
a p p a r a t u s which catalyses the temperature-itisensiti\'e processes of light absorption, excitation energy transfer and
p r i m a r y photochemistry, and which is present (as assayetl by photosynthetie pigment per unit biomass) in smaller
relative a m o u n t s d u r i n g resotirce-sattirated growth at lower temperatures. T h e i i n o h etnent of other low-
t e m p e r a t u r e ' a d a p t a t i o n s ' (e.g. h o m e o \ i s e o u s behaviour of thylakoid membraties) in ofTsetting low temperature
efTects oti catalytic rates is not clear. T h e scope for increasing the qtiantity of temperature-sensitive catalysts m the
b i o m a s s as a means of offsetting the effects of low t e m p e r a t u r e on resource-saturated // is potentialh' higher in the
D i n o p h y t a with their relaln'cly low//^,, at their t e m p e r a t u r e o p t i m u m ; however, this option does not appear to be
t a k e n up by the Dinophyta whicli have unexeeptional *, values for //,.

* Prcsunt adchx-ss: College ol Miuitle Studies, University of Delaware, Lewes, Delaware I')9.S,S-1298, I'S.A.
442 y. A. Raveri and R. J. Geidcr

I-Or resource-limited growth, the phenotypic effect of suboptimal teniperatiucs on growth, when hght is the
limiting resource, is often less marked thiui when growth is light saturated. When a chemical nutrient is limiting,
the tetnperature effect on growth of a given genotype is often, but not invariably, decreased. Cases m which the
i'ffect of temperature on growth rate is decreased under light-lirniling conditions c^^\^ be interpreted in terms of
the intrinsically low (J,,, of growth when temperature-insensitive reactions (light absorption, excitation energy
transfer, primary photoehemistr\') are limiting and the acclimatory effects of changed temperature and light
regimes for growth on resource allocation between pigment protein complexes and downstream catalysts of
temperature-.sensiti\ e reactions. C ases in \sbich light-hmited growth rate is (]uite temperature sensitu'e may be
accounted for by a decrease in absorptance as a restilt ol a lower pigment content per cell at low growtb
temperatures. l'"or growtb limited by cbemical nutrients, the variable responses make analysis dilticult. It is
tempting to assign a low (^m for /( under these conditions to a limitation by some transport process (diHusion
through unstirred layers, or, less plausibly, tbe cell membrane) with a low O,,,, altbougb tbe evuience favouring
tbis interpretation is not abundant.

I^e\' words: /Xctivation energy; HaeiUariophyta, C hlorophyta; I)ino]~)hyta; resource allocation; specific growtb

componctits (indivickial catalysts; lipids in mem-

I . 1 NrHODt:(TI()N
I'eniperature is perhaps the tiiost widely measured
enx'irontnontal variable that effects alpal growth.
Voj^el (l')81) suggests thaf the ease ol measurement
of temperature has Icil to an overemphasis on
temperature in ecology, iti contrast to such less
readily measured parameters as fltitd movement
relative to organisms. It woiilci clearly bo hypocritical
for us to deny the importance of the ' Huid mo\c-
metit' cause espoused by Vojj;el (e.g. Raven 1086,
l')88; MacFarlane & Raven, 198.=;; Raven, Beardall
& (jriflifbs, 1082). Nevortholess, temperature is an
important aspect of the I'cology and physiology of
algae. Temperatiire is almost itivariably measured
and cotTtrolleti in cxperimentai studies etiiplo\ing
algae. However, gencrali/.ations regarding the effects
of tetnperature on mtcroalgai growth ha\'e not
progressed greatly beyonti the descriptions by
F.pplcy (1072) ol an enx'elope ol //, lor a range ot
microalgae as a function of temperatttre. .Vlany
studios of interacting efiects ot temperattire and
other environmental variables (salinity, photon fUix
tletisity, tiutrient ax'ailability) on microalgal growth
provide a vvealtli ot descriptive data, l.'nfortunatcty,
most of these data are largely uninferpretable in
terms of recetit advances tn the tnechatiistic descrip-
tion of algal growth (Shutcr, 1079; Kiefer &
Mitchell, 1083; Raven, 1076, 198(), 1982, 1984,/>,
1986, I987). We wish in this paper to discuss
some principles which relate to fhe study of the
elfccfs of tcmpcratitrc on algal growth.
We start by discussing some of fhe differctitial
ctTects which a change in futnperaturc niighf have, in
the absence of any adaptation or acclimation, on
metabolic processes. We subsec]uently discuss how
these differential effects can be accommodated in
resource-saturated, and resource-limited algae. The
two responses which vyill be considered are those of
(I) changes in the properties of the catalysts of
particular reactions, or of membrane lipids, and (2)
those related fo changed ratios of the various cell
brane; structures and storage cotnpouncls) as a
part of the getiotypic or phcnof\pic response to
temperature.
ir. T H I ' F. I ' I ' l ' C I S OI' riiMl'l- l-tATl'HI- () N
( " M t ' . M U A I , T RA N S l ' O H M A l l ON.S A N D O N
T R A N S l ' O R T I ' R ( ) f l i S .S ! S , A N D i'OSSIlU.F.
\1 I - f It A.\' I S M . S OV A M t ' l , t () R A t t N ( ; T H I- I R
I s l ' l ' t; C T S O N At.(;Ai' A T 1 , ( ) W f I", \ l f t i R A T I I R I". S
1. 'rciiiperdtiirc cjfecl on ciitiilysed and uncatalysed
flwmical transformation and transport processes
Here we deal briclly with some of the effects which
temperature changes ha\ c on chemical and tratisport
processes of importaticc to organisms exclucling
those which may be tcrtncci ' acchmation ' or ' adapta-
tion ' on the part ot the orgamstn, and also not
dealing with any temperaturc-rclafcd breakdown iif
catalysts or structures (sec Johnson & 'rhortile\ .
1085).
Fable 1 summari/.cs sotnc temperature effects on
chctnical transformations and transport processes.
As befits a paper dealing with photoroplis, we start
by pointing out that light absorptioti, excitatiiin
energy transfer, and photochemistry are temperature
independetit. I'or chemical rcactiotTs, the cxatiiple of
catalase reminds us that the temperature effect on an
uncatalysed reaction is greater than that for a
catalysed reaction; iti this case, inorganic catalysis is
more temperattire dcpctident than is the cnzymc-
catalysed process. It is important to remember that,
ot cnzymc-catalysed reactiotis, \-{.,()., brcakdt)wn to
ll.jO and O., is (with the reactions catahsed by
superoxide dismutase and carbonic anhydrase) an
exception in that it bas a low enough actixation
energy to have a sigtiiticant ttncatalyscd rate. Flolland
(1980) tabulates the rate of the catalysed relative to
the uncatalysed hydration of C.'O^ b\- httman red
blood cells; the ratio is 4()()() at 42 C and rises to
at 12C. As bctits the role of enzymes iii
 Temperature atid alf^al groivth 44.1

T a b l e 1. Acltration cneri/y and y,,, values for some processes relevant to iirou-th of ornanistns. Data chosen to
illustrate intrinsie effeet of temperature on tiie process roith no aeelimation due to ehaniie m amount of kind of
catalyst, or altered nienihratte lipids

Process (1<J mol ') Referetices

(1) Photochemistry
Photochemical processes 0
H,,O., - H.O -^ '<>:! (uncataiysed) 75
H.'Oo - H.'O -+'-SK(catalysed by 54 Cioodwin & Mercer
coilotdal Pt) (1983)
H,,O., - l-l.A) --> -.O.. (catalysed by 29
catalase)

(2) Catahsed and iincatahsed chemical

reactiotis
H \ d r o h s i s of ethyl butyiate with 13 1-2
patTcreatic lipase
Hydrolysis of solanin with etiiulsin 10 Steam (1949)
Hydrolysis of sucrose with iiu ertase 30
Hydrolysis of sucrose catalysed 109
by H^"
Hydrolysis of sucrose catalysed by 54
malt 'sucrase' Dixon & Webb (1964)
Hydrolysis of sucrose catalvsed by 46
yeast 'sucrase'
1 K'drolysis ot ralhnose t'alalyscd 46
by \ea.s( 'sucrase '

(3) Diffusion 111 aqueous sokition

Diffusion coelHcient in Moroic tuiit'i iianiis
(Teleost) cytosol of
Lactate 45
2-Deox\'nlucose 41
.Stdell & Hazel (1987)
AMP-PNP (-L5)
Diffusion coeflicietits in water 18 7 20 7 Stein (l')86)
(solutes = tracer 11,0, urea, ^lyciiie,
alanine, glucose, cycloheptamylose.
bovin serum albumin)

f4) Membrane permeation (non-mediated and

mediated uniport)
Permeability coefficient of Nitcllupsis
ohtusa (Des\. in Lois) J. (;ro\. (as
Tolypeltosis stclhi^'cra) to
Glycerol (P.,,,,,,, = 2 2 x 10 " m s ') 92
Urea (P.,,, ,. = 2'2 x 10 ' m s ') 70 A Wartio\aara (1942)
Kthylenesfycol (P.,,,,, = 2.8x 10 ' 70
m s ')
2.3-Butylenelyeol (P,,, ,. = 139 6 6
4-4 X io ' tn s ')
Trimethylcitiate (P.^,, ,. = 4 4 x 10 ' 126 Wartiovaara (1942)
m s ')
Kthylurethan (P^,, ,, = 0-02 m s ') 81
Pertiieability coellicient of horsebean 55 2 1 RossiK 11(1il, L'so & '1 honias
phospholipid bila\ers to H ' (1985)
Permeability coeHicient/hydraulic 53-55 2 05 2-1 House (1 974)
conducti\ity of phospholipid hilayers
to H.,O
Permeability coelhcient of Dunaliella 15 5 1 23 DeRani .S: .Avion (1982)
salina Toed, plasmalemma to H.,()
Hydraulic conductivity of NitelUi 35 7 1 62 Dainty & CinzbuiK (1964)
translucens (Pers.) Afi... em., plasma-
lemma
Permeahilit>- (conductance) of K' 36 (ah()\e 15 C) 1 631
Homble (1985)
channels ol Cliarii corallinti Klein 50 (below 15 C) 1 9 7 /
ex. Willd, em., plasmalemma 25 1 40 Smith & Kerr (1987)
444 J. A. Raven and R.J. Geider

T a b l e 1. (tonl.)

Process (kJ mol ') Referet-ices

(5) I'rin-iaiy active transport at plasma-

Priinary active 11^ efflux (measured 44 (mean of 18 K a m i - i k e et al. (1986)

as conductance) of Chara eorallina 6 28 C)

(6) ,Microalgal growtb, photosyntbesis,

enzyme activity
Carboxylase activity of R U B I S C O 72 (0-40 C) 2-66 Descolas-CIros & D e Hilly
from Phaeodfiilyliini tricoriiuttnii (1987)
Bohlin ('ten-iperate d i a t o m ' ) and of
Nitzschia kerguetcnsis O'Meara
('antarctic diatom ')
Nitrate reductase activity in extracts 38 (5-15 C.') 18 K r i s t i a n s e n (1983)
of Ileterocapsa triquetra (l'"brenb,)
Stein (a dinoflagellate)
/i^^^ i,( Phaeodactyluin tricorniitiini 3 5 (5-15 C') 35 ^
Bohlin
Light, C(),,-saturated photosyntbesis 70 (5-15 C;) 2-66
of Phaeodactyliim Iricorniitiini
Bohlin Li & M o r r i s (1982)
Carboxylase activity of R U B I S C O 54(5 15 C) 2-07
from Phacodactyluni tncormitiini
Bohlin
Phosphoetiolpyruvate carboxylase 54 (5 15 C) 2-07,
activity of Pliacodactyliini tricorii-
iitiiiii Bohlin extracts
Natural marine pbytoplankton popu-
lations from the arctic
Light-saturated photosynthesis 70-6
R L ' H I S C O carbox>-lase activity 723
Pbosphoenolpyruvate carboxylase 326 Li, S m i t h & Platt (1984)
activity
Pbosphoenolpyruvate 25-1 1-4
carboxykinase activity

(7) Respiratory of microalgae

Respiratory electron transport
capacity in vitro in planktopbytes
grown iihotolithotrophically at
1 X ('
Pliacodactyliini triconiiitiini Boblin 38-9 1-79
SkcU'tonenia castatiini ((Jrev,) 45-1 1-97
Cleve
Chactoccros dchile L'\L-VI: 51-0 215
A h m e d & K e n n e r (1977)
Cyclotetla sp, 68-6 280
Cricospliacra cartexic (Braarud & 49-7 210
I'Liger,) Braarud
Dunaliella tertiolecta Butcher 51-0 2-15

(8) 'l'bylakoid reactions

Non-cyclic electron transport in 55-5 2-12')
Spinacia oleracea L, (llowering plant)
tbylakoids (I I./) - ferricyanide; coupled)
Non-cyclic pbotopbospliorylation in 55-6 2-12
Scburmans </ ,;/, (1984)
Spinacia oleracea thylakoids ( H , / )
- ferricyanide); cyclic photophos-
phorylation (pyocyat-iinc as catalyst)
ATI* hydrolysis by light-and D T H - 53-1 2-03,^
activatetl chloroplasts ol Spinacia
oleracea
Initial rate of IL net inlUix at ligbt 285 1-53 Yainamoto & Nishin-iura
saturation illumination of Spinacia (1976)
olcracca thylakoiils in the presence
of a catalyst oi cyclic electron trai-isport
(I'hetiazine inetbosulphate)
 Temperature and algal growth
Table 1. (cont.)
Interconversion of /? and (), used the following equation (Dixon & Webb, 1964, p, 1.S7):
T^
10
where R = gas constant (8-3 mol ' K '), T = absolute temperature (K) (mean for range oxer which (), was measured),
E.^ = activation energy (J mol '),
Computations of /? from plots of log,, rate versus the reciprocal of tbe absolute temperature used the relationship
r^ R \T, r.J
where r^,r.^ are rates of reaction at temperatures T], T.,, and T, > T); temperatures in K,
reducing activation energies, some enzyme-catah-seci
processes have very low activation enerjjies and
hence low Qj,, values (e,g, three of the six hydrolases
quoted in Table 1),
OifTusion coefficients in aqueous solution, or in
cytosol, have Q,,, values which overlap with the
lower end of the 'enzyme' range (Table 1),
T h e permeability coeflicients for solute transjiort
through biological membranes by the tincatalysed
route (lipid solution) have relatively high tempera-
ture coefficients since, in adciition to temperattire
sensitivity of difTusion within the membrane, there is
a temperature efiect on partitioning into the mem-
brane from aqueous phase (see Stein, 1986), The
activation energy for entering the lipid phase is
greatest for the less lipophilic molecules, so there is
a negative correlation between the permeability
coefficient and the Q^^^ when a range of compounds is
considered (Table 1), Water transport across man>-
biological membranes often has a higher O,,, xaltie
than does its movement across hilayers constructed
in vitro from natural membrane Iipids (Table 1),
For the mediated transport processes. Table I
again shows a substantial range of values, with no
clear distinction between the \-ariotis kinds of
transport [the categories of primary aeti\-e uniport,
passi\'e uniport ai-id secondary acti\-e transport, i,e,
antiport and sytnport (Mitchell, 1977)], or between
mediated anci non-mediated transport. The range of
Q^ values for mediated (catalysed) transmen-ibrane
fluxes is similar to that for enzyme-catahsed chem-
ical transformations. If tbe enz\-me-calalysed re-
actions were to be categoriy.eci in the san-ie manner as
mediated transmembrane Huxes (Mitchell, 1977), we
Aould again find substantial o\-erlap between the
\-arious groups of enzymes. We note that, in general,
the uncatalysed rate of transmetnbrane mo\-ement
by cotnpounds subjected to meciiated transport is
negligible, as a result (as with en/.yme-cataKsed
reactions) of a \-ery high activation energy.
It IS of interest that, where the same process lias
been examined in different organisms, there are
often variations in the effect of ten-iperature. Before
too much is made of this, especiaffy when different
445
in\'estigations are involvecf, it must be borne in mind
that different investigations using the sai-ne organism
(but probably not the same strain) n-iay prodtice
different temperature effects. An example is
RUHISCO (ribulose bisphosphate carboxylase-
oxygenase) carboxylase activity from Phacdactyhini
truornutum Bohlin (see Table I),
Not included in Table 1 are temperature effects on
mobility phenomena in algae. The reason for this is
that the temperature effect on cytoplasmic streaming
and on cell moven-ient mediatecf by Hagella is not an
exponential 'Cm' relationship, L'mrath (1934)
showed that the \-elocity of cytoplasmic streaming m
Nitella mticronata Mitjuel, was a linear function of
temperattire in the range .S- 20 C (see pp, I 66 I 67 of
Mope & Walker, 1975), It has been shown that the
change in \-iseosity of the cytoplasm with tempera-
ture is responsible for this effect (Hope & Walker,
1975, pp, 166-167), Kamykowski & McCollun-i
(1986) showed that the swimming velocity of 11
species of marine dinoflagellates, on the low -tempera-
ture side of the optin-ial ten-iperature, either declined
linearK- with decreasing temperature or showed a
greater decrement in swimming velocity per unit
decrease in temperature at lower temperatures.
Thus, both the actin + myosin-based eytoplasmic
streaming and the ttibulin + dynein-based fiagellar
nio\-ement show ' non-Arrhenius' temperature
effects. It is unlikeK- that the \-elocity-ten-iperature
relationsiiip results from a multiplicity of Arrhenius
segments with lower /s',, values for succeeding
segments as the temperature is increased.
We see that the influence of temperature on the
rate of catalysed and uncatalysed reactions which are
important to algal growth is rather \-ariablc. These
effects we dernote as the intrinsic properties ol the
catalysts and barriers (and, by extension, of struc-
tural and storage components),
2, Mcihanisnis ivhcrchy the cell can anicliordtc the
I'ffi'cis of hnv teinpcraturc's
T h e discussion II, (f) above shows that there is a
substantial range in the effects of temperature on the
446 J. A. Raven and R.J. CJeider

rates ot chemical transtormations (mainh' enzyme //, at any gi\en temperature was lower for tbe
catalysed) which are important in algal cells, and in stead\-state cultures than tor tbe batch cultures
the rate o! transport processes in tree solution and considered by I'>ppley (1972).
(catalysed and uncatalysed) across membranes wbich It is important to recognize tbat tbere are
could be related to algal growth. If the catalysts and important efleets otber than temperature on /(,,,.
membrane lipids through which uncatalysed trans- Banse (1982) has made a careful analysis of literature
port occurs are both qualitatively and quantitatively on the relation of //,,, to cell size in diatoms anci
unaltered, then a decreased temperature for growth dinophytes, 'corrected' from the actual growtb
will prodticc an unbalanced array ol rates ot chemical temperature to the //,,, at 20 C, using Fppley's
reaction and of transport. Thus, the rate of growth at (1982) genotypic value for Q^ of//,,, of 1-88. Banse
the lower temperature may be limited by some (1982) demonstrated two important features of tbe
ixirticularly temperature-sensitive process. This limi- effect of phylogeny and cell size on 'temperature-
tation would not be so pronounced il eitber the corrected' //,,,. For cells of a given size, dinophytes
properties of the component change such tbat its grow less rapidly than diatoms. For cells from a
capacity at lower temperature is increased, or given class (Dinophyceae or Baeillariopbyceae), //^^
allocation is altered sucb that the quantity of the decreases with increasing cell size, albeit with a
limiting component is increased relative to that ot lower size-dependence tban for many non-pboto-
other components of the catalytic structural storage synthetic organisms (e.g. the ciliates and rotifiers
apiiaratuses ol the cell. considered by Banse, 1982, in parallel witb tbe
Our discussion of tbe mechanism of genotypic or microalgae). Raven (1986, I987) tabulates tbe //,,,
pbenotypic acclimation to different temperatures values ('corrected' to 20 C with a (), of 2) for a
will accordingly relate to two major possibilities variety of phototrophs of different cell sizes, although
wbicb are not mutually exclusue. One is that ot most of the data for eukaryotes other than diatoms
molecular changes in catalysts or lipids such that and dinophytes come from members of the Cbloro-
their ability to bring about the appropriate chemical phyta. This analysis suggests that //, values of
change at a lower temperature is higher than would eukaryotic phototropbs otber tban members of tbe
otherwise be so. This might involve (for catalysts) a Baeillariopbyta are no higher than those of members
rci:)lacement of a form of an enzyme or transporter of Bacillariophyta of the same cell size at 20 C.
by a \ ersion wbich has a higher activity under //( vivo In considering the interactions among the tax-
conditions at the lower temperature, or an increase in onomy-temperature-size triumvirate on //,,,, two
the degree of unsaturation wbich would maintain points must be emphasized. One is tbat, in a giveti
N'iscosity and (probably) permeability by lipid- taxon (algal division or class), not all representati\ es
solution mechanistns, constant. The other category of a given cell size attain the temperature-corrected
of possibilities is a reallocation ol resources sucb //,,, found tor the fastest growing members. T b e
tbat, at lower temperattires, the more temperature- second is that there is an element of circularity in the
dependent components are present at a higher use of Eppley's (1972) Q,,, for /;, in different
relative concentration that! the less temperature- genotypes uncorrected tor etlects of cell size or of the
sensitive components, (jeneral discussion ot the major taxon to which the genotype belongs, to
acclimation of organisms to various temperatures correct the//, values for cells of a range of sizes and
may be found in Moebacbka & Somero (1984) in the belonging to different divisions, to tbe value to be
context of ectothermie animals. expected at 20 C. However, it would seem that tbe
errors ititrodticed in this way are not large. Tbe
range of cell sizes in the genotypes from wbich
M l . r i l l - o i i s i ' K v i ' I ) i: ! ! i; c T o i ' r i : M I M ; u A r t ;
Fppley (1972) deduced the (Pm of//,,, was not large,
O N H1',S()IM(CI.-SA r U H A T I H ) A L C A I . C K O W T I I
especially when cotisidered in relation to tbe rela-
I'.ppley (1972) has reviewed the etfect of temperature tively small size-dependence of//,,, within a gi\-en
on algal growth. For batcb cultures ot a range of taxon.
diatotns and green microalgae he showed (fig. I of At the phenotypic level, it is eommonly found
Ivppley, 1972) that //,, at tbeir respective tempera- (Fppley, 1972) that the (y;,, for growth of an individual
ture optima, tor a range ot genotypes had a Q,,, of genotype at temperatures below the temperature
1 88. The 0,(1 '"r I'm "^ ''" individual genotype at optimum is greater tban the Q^ of //,, at tbe
temperatures below tbe optimum was greater than respective temperature optima, of different geno-
188. In other words, the phenotypic effect of types. This suggests, perhaps, that a single genotype
temperature on //, was greater than the genotypic is often less good at growing with a high specific
effect. CJoldman & Carpenter (1974) undertook a growth rate over a range of temperatures ( < 20 C)
similar analysis for microalgae growing in ebemostat than are several genotypes. A low phenotypic Qj,,
cultures, and deduced (depending on wbicb data sets olten correlates with //, values lower tban tbose
thev included) (y,,, values of 2()8 2-19. In addition to tound for a faster growing genotype (of similar size)
the rather bigber (P,,, valties, tbe absolute value of with a sharper temperature optimum (e.g. Stephana-
 Tentperature and alf^ol f>roicth 447

discus miiuttis Crun.: Mechling & Kilham, 1982). in these cases (Raven, 1987<v, p. 322). It is also
W e note that, phenotypically, j^ross cell composition important to note that some of the essential cataK'sts
is n o t generalK' much altered by growth temperature of growth bring about a loss of C (e.g. essential
(e.f^. measured by C/N ratio: Cjeider, 1987; Li, biosynthcses in\ oh ing decarboxylation) which must
1980; Verity, 1981 ) so that the tiualitative and also be accommodated.
quantitative requirements lor biosynthesis per unit In steady-state growth all of the transport pro-
C assimilated are essentialh- temperature-in- cesses and chemical reactions which contribute to
dependent. This conckision accords with the obser- growth must proceed at rates appropriate to pro-
vation (Verity, 198I./), I982,i) that the specilic duction of cells of the observed Hnal composition.
rate of dark respiration (a process which usualK' has However, some catalysts are more growth-limiting
a major biosynthetic component) in lA'ptocyliiuirus than others. Sensitivity analysis (Raven, I987,
daniciis Cle\'e is a constant traction of the specific p. 333) is the best method of determining which
growth rate [both in units of mol C (mol cell C) ' catalysts arc most growtli limiting (i.e. ha\e the
s '] at 20, 15 and 10 C (although not at 5 C). lowest product of R and R). In practice such analyses
However, Verity (1981c;,/;) found that the specilic are difiicult at the whole cell level (Kell, 1987) and do
carbon excretion rate was temperature-independent, not seem to have been attempted with algae (Raven,
being a greater fraction of //, at the lower grow th 1987). Some idea of which catalysts are closest to
temperatures. limiting growth can be arri\ ctl at fiy looking directh'
at the product of B and R. .A small product implies
[equation (l)j a high \alue for /'', i.e. there is iittlc
I\'. EXPLANATION O I' Tin- !: 1-'I'! (' T S Ol' spare ca)5acity.
T E M F l ' R.AI'L' H V. O N lil':.SOr KCI'>.S ATU R.ATl':!)
Raven (1984, 1986, 1987(;) suggests that the
.-\LGAL GROWTH
obscr\ed //, for small diatoms and green algae arc
O u r attempt to explain the effects ot temperature on within a factor of two of the maximum which could
resource-saturated growth are underpinned b\- con- be expected, granted the following assumptions.
siderations of the teni)ierature dependence of the (1) R \alucs for homologous catalysts ol a par-
allocation of resources between \arious liinctional ticular reaction are essentially lixed quantities. Tliis
components of the- alga and the kinetics of the assumption finds support in tlic obserx ations that no
catalytically acti\'e components of the cell (sec dramatic changes in R for RL'HISCO, the cyto-
Shuter, 1979; Raven, I976, 198(), 1986, 1987; chromc Z;,. / comiilex, the .ATI' synthetase comjilcx,
Geider, 1987; Geider & Flatt, 1986; (;eider, Platt & or ribosomes, can be invoked on the basis ol
Raven, 1986). comparisons of microalgae with other organisms.
At a given temperature, we can (Raven, I987) Where analogous (as opposed to homologous) cat-
equate the maximum specific growth rate, /(,,j, for a alysts occur, e.g. plastocyanin/cytochromc r, or
cell to the product of the fraction of the cell occupied ferredoxin/fla\'odoxiii, there arc no ver>' large varia-
by a given essential catalyst, the maximum specific tions in the R \ aluc.
reaction rate of this catalyst, and the fraction of this (2) The value of B for a given catalyst can be
specific reaction rate which is expressed /// 7'ii'<), increased by either decreasing the B \ alues lor one or
thus ; more other catalysts or decreasing the allocation ot C
//, =BxRxF, to some other (non-catalytic) cell component sudi as
where storage materials or to structural components (mem-
branes, cell walls, etc).
//^, = maximum specilic growth rate; mol C
The potential for increasing //, by altering the
assimilated (mol C in cell) ' s ' ;
ratios of B values for different catalysts within a
B= concentration of the catalyst in the biomass;
gu'en fractional allocation of cell C to catalysts is, at
mol C in the catah'st (mol C in cell) ' ;
constant R \ alues, constrained by permissible \ alues
R = maximum specific reaction rate of the
of F [sec assumption (3) below]. Clearly, if//,,, is to
catalyst; mol C transformed by the cataKst
be increased by increasing B for catalysts which
(mol C in the catalyst)"' s"';
already have high F values, then the catalysts whose
F = Fraction of the maximum specific reaction
B values are thereby decreased must attain their
rate of the catalyst which is reejuired to contribution to a higher //,,, by higher values of / ' .
account for the measured //,. The implication is, that if/^,, is to be increased above
It is important to note that the definition of R can, the observed ceiling, a number of catalysts must have
and must, be applied to substrates that do not low F values in 'real' organisms which could be
contain C (e.g. photons tor light-harvesting pig- increased in the hypothetical rapidly growing organ-
ments; NO.)" for NO3 transport catalysts and NO., ism [see assumption (3) belowj.
reductase) and substrates that contain C which is Increasing //,,, by increasing the fraction of cell C
not directly involved in C transfer from CO., to end- which is allocated to catalysts implies that some C in
products. Appropriate scaling factors must be tiscd structures and/or reserve materials can be deleted
448 . A. Raven and R.J. Geider
without decreasing //,,,, There seems to be little scope
for decreasing the C^ allocation to structures such as
membranes if their barrier functions, and the
activities ol the catalysts in or on them, are to be
maintained (e,g, Ra\-en, 1984c(), There is some scope
lor decreasing C allocations to structures such as cell
walls and to storage compounds provided a constant
enMronment can be guaranteed. In the absence of a
constant environment the organism is at risk from
osmotic downshock if the safety margin of pressure
tolerance of the wall is lowered, and from energy
star\-ation if the content of C/energy reserves is
decreased (see Raven, 1982, 1987/)),
(3) The value of /'" should be close to 1-0 if the
organism is to i-i-iaxin-iize the return (in terms of //,)
on the investment in catalytic machinery. However,
considerations of controllability of metabolism re-
quires a range of F values (Heinrich, Rapoport &
Rapoport, 1977),
The available evidence accordingly, suggests that
the fastest-growing diatoms and green algae are close
to the limit on /', for photosynthetic micro-
organisms. If we consider a photosynthetic micro-
organism whose /(, (at the optimal growth tempera-
ture) cannot be increased by reallocation of re-
sources between catalysts, or between catalytic and
non-catalytic components, we can examine a simpli-
fied case for the change in //, at temperatures below-
the optimal temperature,
(jrowth (under optimal resource supply condi-
tions) of such an organism at a temperature below its
optimum will be significantly constrained by tei-npera-
ture effects on the value of R |equation (1)] of its
organic catalysts. Any non-photochemical catalyst
exhibits a signilicant temperature effect related to the
supply of activation energy for populating the
'activated state' of the catalyst substrate complex
from thermal agitation, (We shall mention the
generally lower temperature effect on catalysed than
on non-catalysed reactions later,) Accordingly, the
entire suite of catalysts of processes downstream
from the primary photochemical reactions of photo-
synthesis will be slower at lower temperatures. Light
absorption excitation energy transfer and primary
photochemistry are, in contrast, temperature inde-
pendent. Thus, if an organism is to allocate resources
optimally between catalysts at a lower temperature,
it should decrease the fraction in the temperature-
independent catalysts of light harvesting and pri-
mary photochemistry (whose R values are tempera-
ture-independent) and increase the fraction in the
downstream catalysts with temperature-dependent
R values (see (ieider, 1987), An increase in 0 (the
ratio of total cell C to chlorophyll a per cell) is
observed as both a genotypic and a phenotypic
response to lowered growth temperature (Cieider,
1987), This is consistent with an increase in the
content of thermochemical catalysts relative to
photochemical catalysts (content = B values). It
should be noted, however, that the total cell C
component of 0 involves non-catalytic (structural
and storage) C as well as catalytic C, and tbat the
relative contributions of these two pools to change in
I) with temperature has not been investigated. It is
important to note that this eflect is significantly
n-iodified by \'ariations of photon flux density, being
more pronounced at high photon flux densities of the
type considered here as resource-saturated growth.
Our predictions as to the effect of decreased
temperature on the resource allocation to structures
are based on an assumed constancy of cell size and
shape during growth at different temperatures. The
assumption of constancy of cell size, despite changes
in temperature for growth, is not entirely realistic
(e,g, Rhee & Gotham, 1981), Dealing first with
smaller cells at lower growth temperatures, it is by
no means clear if the genotypic response of increased
//,,, at a given temperature in smaller cells would
apply to a smaller cell phenotypically produced by
lower growth temperature, since the n-iechantstic
basis for the genotypic effect is not clear (Ra\-en,
1986), While a phenotypic increase in cell size at
lower temperatures would be expected, on the basis
of the genotypic responses, to decrease //^^^ at a gi\-en
temperature (Hanse, 1982), again we ha\-e no n-iech-
anistic basis which is widely agreed upon (Raven,
1986), I'Aen if the increase in cell size were all
attributable to an increase in catalytic (as opposed to
storage or structural) components, in cells grown at
temperatures below their optimum, it would not be
possible to conclude that the specific growth rate
would be increased above that which would have
pertained at the lower teinperature had no ii-icrease
in size occurred. In brief, the argument here is that
more catalysts in a cell mean not only that more
substrates on a cell basis can be transformed in a
given time, but that many (if not all) of the additional
substrates would be used in synthesising the extra
catalysts in the given time; accordii-igly, there would
be no increase in // relative to a cell which did not
increase in size at lower growth temperatures.
Assuming a constant cell size and shape at lower
growth-temperature, the near-constancy of cell
turgor pressure with variations in temperature
(Wildervank, 1932; Raven & Smith, 1978a) mean
that the same cell wall thickness (assuming constancy
ol wall composition) is required to give the same
safety margin (see Raven, 1982, 1984a, 1987 6V
Similar arguments apply to the microtubules which
maintain cell shape in n-iany wall-less cells (see
Raven, 1982), These considerations suggest that the
resource use per cell in walls and cytoskeleton should
be similar at difierent temperatures.
With respect to reserves, it could be argued that, at
lower temperatures, the rate of consumption of
organic C in maintenance, or in tiding the organism
over an imbalance of light (low) and nutrient (high)
supply, would be lower. Hence, if the selectively
 Temperature and alircil grozuth
important factor is the time for which the reserves
last, the organism at the lower temperature might he
expected to ha\'c a smaller fraction of their total C
allocated to carbon reser\es (cf. Cohen & I'arnas,
1976; Parnas & Cohen, 1976). However, if we lake
the intercept at // = 0 of a plot of specific respiration
rate z^s. // as a measure of the maintenance metabolic
rate, then the data of Verity (1982c;) sugRest a
relatively small efl'ect of temperature. If this main-
tenance respiration rate is controlled, \ia classical
respiratory control, by the rate of ATP use, then the
rate of ATP use in maintenance processes in
Leptocvlindriis danieiis is not much decreased hy
decreased temperature. We note that the essentialK'
temperature-invariant stoichiometry of specific
growth rate and the specific rate of growth-related
respiration, accounts, again \'ia respiratory control,
for much of the temperature dependence of the
respiratory rate of algal cells under conditions in
which growth is occurring (Verity, I982). To this
data on L. danieus can he added the work of French,
K o h n & Tang (1934) on Chorella enieisonii Shiraha
& Krauss (as Chorella pyrenoidosa). These workers
grew Chorella photolithotrophically at 20-22 C in
continuous light, and then measured respirator)'
rates in continuous darkness over 47-60 h for cells at
temperatures in the range of 0-6 28-0 C. If the high
initial rate is equated with growth-related plus
maintenance respiration, and the lower final rate
attained at ~ 25 h at all temperatures is equated with
maintenance respiration, then it is again seen (fig. 7
of French et til., 1934) that maintenance respiration
is less temperature-dependent than is growth respira-
tion. It should he noted that, if classical respiratory
control holds, then the data of Verity (1982(7) and of
French et at. (1934) do not inform us directly about
the change in respiratory eapaeity as a function of the
temperature at which the alga was grown, or was
maintained over a long period in a non-growing
state. Data of Ahmed & Kenner (1977) on the effect
of temperature on respiratory electron transport
rates in vitro for phytoplankton cells grown at 18 C
in continuous light quoted in '(\ible 1.
T h e allocation of cell C to soluble organic
compounds, e.g. the polyols, glycosidcs, etc. which
a re categorized as'compatible so lutes 'is now generally
considered to be a skeletal/structtiral function rather
than a reserve, at least when the solute is located in
the cytosol (see the excellent work of Davison &
Reed, 1985; and the review by Raven, I987().
.Accordingly, we would expect these cytoplasmic
solutes to be present at constant quantities despite
changes in temperature. Other cytoplasmic solutes
(enzyme substrates and effectors, for example)
would also be expected to be present at essentially
temperature-independent concentrations. Falkowski
n 9 7 7 ) showed that the energy charge of Slwletoneina
costatuni was essentially independent of temperature
in the range 2-30 C despite a more than 10-fold
449
x'ariation in specific growth rate. It is likely that the
free energy of ATI' hydrolysis (related to the energy
charge via, inter alia, the cytoplasmic P, (inorganic
orthophosphate), Mg'"^ and 11' acti\ity, and, conse-
quently, less readily measured) is also conser\'ed (ct.
Gnaiger, 1987). Data from Chara corallina Klein ex
Wild, em., show a slight increase in cytoplasmic pH
as temperature decreases which (unlike the situation
in most ectothermie animals) is not suflicient to
maintain the fH*]/|()H ] ratio constant, and the
ionization state of amino compounds, constant as
temperature changes (Ra\-cn & Smith, 1978/)).
These considerations of homiostasis are consistent
with an emphasis on the constancx' of the pliNsico-
chemical en\ironment of enzymes (and of membrane
transporters) with variations in temperattire such
that (for exatnple) the free energy of hydrolysis ot
ATP, and of oxidation of NAD(P)H, is maintained
much more nearly constant with variations m
temperattire than is //,. The same goes (perhaps to a
lesser extent) for the value of the A/y,,- at the
plasmalemma of (liara corallina (Ra\en & Smith,
1978/); Kami-ike et al., 1986).
One factor of potential importance in determining
reaction rates is the \iscosit\' of the Huid medium
surrounding soluble enzN'mes (i.e. tbe aqueous
cytosol, plastid stroma, or mitochondrial matrix) or
integral membrane polypeptides, incltiding porters
(i.e. the lipid phase of the membrane). Since a likely
evolutionary outcome of selection for maximal
catalytic capacity of an enzyme t)r transporter is
diffusion limitation of the reaction rate at low
sttbstrate concentrations, and Htiiti kinematic vis-
cosity is a major determinant of difftisive resistance
m that fitiid, we might expect viscosity changes with
temperature to alter some reaction rates (see Sidell &
Hazel, 1987; Tyler & Sidell, 1984; Jones, 1986;
C'legg, I 984, for discussions from a non-phycocentric
viewpoint). Clearly not all reaction rates of catalysts
are likeK- to be dilfusion-limited (cf. lleinrich et al.,
1977).
For vertebrate (ectotherm) cytosol, Sidell &
llazell (1987) found, between 5 and 25 C, a O,,, for
kinematic viscosity of 1-35 + O-O1, and Q^, values (or
the diffusion of lactate of 1-84 0-36, 2-dcoxyglucose
of 1-75 0-54, Ca'+of 2-04 0-36, and for AMP-PNP
(an ATP analogue), 0-98+ 0-12 (sec Table 1). It is
clear that the temperattire effect on viscosity is
similar to that found in ptire water (though the
absolute valties are lower than in water), so that the
cytosol has no special properties which decrease
temperature effects on viscosity. The diflusion
coefficients for small molectiles are lower than those
in free solution (0-2 0-4 of free solution values at
25 C) and, with the exception of AMP-PNP, have
higher (), values. Limitation of the rate of metaholic
process by diffusion of lactate, glucose or Ca'*
would, then, yield 0,,, values (1-75 2-04) similar to
that of the ), (genotypic) for microalgal //,. The
450 J. A. Raven and R.jf. CJeider
negligible temperature dependence of the diffusion
coefficient for AMP-PNP may be very significant in
view of the possible limitation of metabolism by
diffusion of the ATP-.'^DP-P, system (Wilson,
Nishiki & ICrecinska, 1981 ; Jones, 1986). The origin
of the very low temperature coetticient is attributed
by Sidell & 1 hizcll (1987) to changes in the ionization
state with temper;Uure ot cytosol, since the pK.^ of
phosphates increases much less with temperature
than docs cytoplasmic pM of ectothermic animals
(White and Somero, 1982). .Algae apparently have
lower cytoplasmic pll increases as temperature
decreases than to ectothermic animals (Ra\cn &
Smith, l97Hh), but an eHcct in the 'correct' direction
(decreasing (_-*,,, for ATP diflusion) would still
occur.
I''or the lipicl phases of membranes, by contrast,
there is evidence in some membranes ot some
organisnis (e.g. the ihylakoid membranes of Pisum
sativimr. Mitchell & Barber 1986; Barber et al.,
1984) for ' homcoviscous adaptation' (see Hochachka
& Somero, 1984). By changing the lipid composition
of the membrane its viscosity, and hence the
diffusion cocHicicnt for molecules dis.solved in it, is
held essentially invariant with temperature. I'his
constancy is important for non-mc-diatcd lluxcs of
solutes (by 'lipid solution') across the membrane,
for lateral interactions between membrane proteins,
and for the lateral and transverse fluxes of the
quinonc ciuinol couples UQ/UQII,^ and PQ/PQI I.,.
P Q / P Q l ' j diffusion, connecting the redox activities
of the pliotoreaction two complex with those of thc
cytochrome /;,; ,/ complex, might be a limiting step in
photosynthesis (ISarber, 1982) at light saturation,
although reactions at or within the cytochrome 6,.-/
complex are also possibilities for limiting the redox
capacity of thylakoids. 1 lowcver, data of Cjombos et
al. (198S) on the effects of catalytic hydrogenation of
lipids in Pisum sativum L. thylakoids do not support
the hypothesis that decreased redox reaction rate in
the PQI 1., cytoehrome /) /complex segment is the
major cause of decreased overall, full-chain electron
transport by this viscosity-increasmg hydrogenation.
Measurements of the ellect of temperature on the
rate-limiting step (the /i for recovery of Hash yield in
intermittent hght experiments) which yielded a (J,,,
of 2-2 in whole cells of Chorella vulf^aris f?eij. (Diner
& Mau/.crall, 1973) were not associated with suHi-
cient acclimatization time for homeoviscous adapta-
tion to occur. The early experiments of Emerson &
.Arnold (t9.12,/;) on Chorella emersonii (as Chorella
pvreiioidosa) were limUed by instrumentation with
respect to measuring turnover times at 20 25 C, but
\-iclded generally similar results tt) those of Diner &
Mauzerall (1973) for their Chorella strain.
Interpretation of the experiments on turno\er
times in flashing light experiments is complicated by
disagreement as to whether the interphotosystem
redox reactions are the major determinants of the
photosynthetic capacity of algae. Sukenik, Bennett &
l-alkowski (I987o,/j) favour RUBISCO activity as
the major factors in Dunaliella tertioleeta Butcher,
while photoreaction two (somewhere between H.,O
and the PQ pool) is also a possibility (Fasham &
Platt, 1982; Samueisson & Prezelin, 1985; Samuels-
son et al., 1983). Photoreaction two is clearly limiting
during photoinhibition (Demeter, Neale & Melis.
1987), and presumably close to limiting under
conditions in which repair just keeps pace with
photoinhibitory damage (Raven & Samueisson,
1986). llowever, the paired Hash technic|ue, which
tneasures the turnover time ol reactions between
W.p and the PQ pool (Mishkind & .\lauzcrall, ! 980),
yields a turnover time in Chlorella luilgaris at 24 C
ol 0-6 ms, while the intersystem turnover time m the
same material at 24 C was 10 ms (Diner &
Mauzerall, 1973). In other words, the capacity for
photoreaction two and associated reaction is, at least
111 transient experiments, more than 10 times that of
the least active catalysis in photosynthesis as a
whole.
Taking these considerations on temperature de-
pendence of \'arious catalysts in toto, it would appear
that the algae growing at lower temperature might be
able to allocate a larger fraction of its cell C to
essential thermochemical catalysts than is so for the
organisms at higher temperatures. This reallocation
would. 111 part, help to offset the effect of a decreased
value ol R [ecjuation (I)] for proteiiiaceous catalysts
in lowering //, at lower temperatures. 1 lowever, the
data on the chemical composition (excluding chloro-
phyll) of microalgae as a function of growth
temperature show little influence (Cjoldman, 1979,
1980; van Baalen & O'Donnell, 1983).
I'^urther ollsets of the lowered catalytic capacity on
a per cell basis could be achieved, independetit of
changes in the gross chemical cotnposition (the ratio
ot components) and without changes in the mole-
cular biology of the components, by changes in the
substrate affinity. .An increase in substrate affinity at
low temperatin-es would go some way to offsetting
the decreased substrate-saturated rate of catalysis.
prinideil that the catalyst operate.s /;/ vivo at sub-
saturating substrate concentrations. This is not an
uncommon feature of enzymes (Hochachka .S;
Somero, 1984; (iraham & Patterson, 1982) in
animals and higher plants, although the reviews cited
also contain counter examples. .An example of ' i\:
adaptation ' in higher plants comes from Teeri (1 980\
who measured kinetic properties of malate dehydro-
genase and of glucose-6-phosphate dehydrogenase
tor populations of a species growing at high and at
low temperatures. The minimum Ki (maximum
affinity) occurred at a 2-5 C higher temperature
than that at which the populations grew.
For the algae, Davison (1987) finds that (as in
higher plants) the /v;(CO.,) of RUBISCO carboxy-
lase activity in the brown macroalga Laminar:,:
 Temperature and algal growth
saccharina (L.) Lamour decreases with assay (but not
grozvth) temperature. However, the A.'i(C()o) of
R U B I S C O is not strictly rele\'ant to resource
saturated growth since CO.^ is, by definition, satur-
ating for RUBISCO activity under these conditions.
Davidson's results will be further considered in
section VI. .More relevant to the present consider-
ations is the A'l value for the other substrate of
R U B I S C O , i.e. RUBP (ribulose bisphosphate). This
has been investigated by Descolas-Gros & De Billy
(1987) for a number of diatoms. There is a decrease
in K^ (RUBP) for a temperature species and for three
antarctic species over some part of the 0 40 C
temperate range. However, at the temperature of
assay is further decreased, the Ki (RUBP) generally
increases again; this increase starts at 20 C for the
temperature species, but at 5 C for two of the three
antarctic species. It is of interest that the minimum
Ki values were found at temperatures very close to
those at which the algae were cultured, i.e. 3 C for
the antarctic species and 18 C for the temperate
species (cf. the higher plant data on dehydrogenases
quoted above: Teeri, 1980). The use of different
growth temperatures for the antarctic species from
that used for the temperate organism means that it is
not strictly possible to conclude that the obserxed
differences in A'l are genotypic rather than pheno-
typic effects. The relevance of these findings for the
in vivo behaviour of the enz\nie is predicated on
RUBP-limitation in vivo; this is generally inNoked
but, as the discussion two paragraphs above shows,
Sukenik et al. (I987rt,/)) favour limitations of
resource-saturated photosynthesis of Dunaliella ter-
tiolecta by RUBISCO carboxylase activity rather
than by the capacity for th\lakoid reactions, and
hence of RuBP regeneration.
These conclusions of changed substrate affinity of
enzymes as assay temperatures is altered only ha\'e
significance, /;; vivo, if the enzyme is not substrate-
saturated. It is clear that the occurrence of stead>-
state substrate concentrations /;; vivo which are
subsaturating for a given enzyme are needed il a
change in Hux through the enzyme is to be
accommodated. .An example of a change lii llux per
unit enzyme is that of photos> nthesis when the
photon flux densitv' incident on the organism is
changed. A further consideration is that, if the
enzyme capacity is to be lulK' exploited //; z'iiu). the
mean substrate concentration must not be too far
from saturation.
Changes in the Ky x'aluc of an enzyme at a gixen
temperature as a consec]uence ol genetie acclimation,
albeit not yet rigorously demonstrated in algae (see
the discussion above of work of Descolas-Cjros & De
Billy, 1987), thus provides another means of suiting
the per cell (or per biomass) capacity of a catalyst to
a different temperature (i.e. a method other than
changed quantity of catalyst, or temperature related
changes in the kinetics of the catah'st). .Another
451
variant on the genetie acclimation is a changed Q.^
(E^) oi a catalyst such that the organism which
normally grows at lower temperatures had a lower
Q,,i, giving a higher substrate-specific reaction rate
for low temperatures but, frequently, lower rates at
higher temperatures. The available evidence sug-
gests that such a change is not found for nitrate
reductase (Kristiansen, 1983) or RUBISCO (Des-
colas-Cii-os & De Billy, 1987) in different algal
genotypes.
We not turn to a consideration of algae whose //,
at their optimal growth temperature is lower than
that f'or other algae of the same size with the same
optimal growth temperature. Banse (1982) showed
that the fastest-grow ing members of the Dinophyta
have lower //, values than the fastest growing
representatives of the Bacillariophyta of the same
size. The Dinophv ta ma>', then, be taken as a group
ot organisms which routinely fail to achieve the //,
values of diatoms (or chlorophytes) of the same size
and with the same optimal growth temperatures.
Analysis of this uiider-achievetnent (viewed an-
throi^ocentrically !) by the Dinophyta in tertns of the
allocation analysis used abovx- cannot, with the
evidence to hand, be achieved with great precision.
However, it does not seem as if allocation of
resources to cell coverings ('aniphiesma ' of Dodge,
1983) or to Hagella, rather than to eatahsts, can
explain the shortfall in //,; neither can the presence
of much more of the cell C^ in reserves than is so for
diatoms or chlorophytes (see Raven, 1982, 1986,
1987 a).
CJeider (1987) points out that the Dinophyta have
a higher value of 0. averaging about three-fold, but
sometimes much greater, than liav e other microalgae
when grown under comparable photon Hux densities
at 20 C. The light-saturated rate of photosynthesis
at 20 C, expressed on a chlorophyll basis, is not
signilicaiitlv' higher in Dinophyta than in Bacil-
lariophyta and Chlorophvta (e.g. Humphrey, 1975).
By no great feat of arithmetic it is possible to show
that the capacity for light-saturated photosynthesis,
on a cell C basis, is lower in Dinophyta than in the
fastest-growing diatoms and green algae. In at-
tempting to trace causal relationships between this
low photosv nthetic capacity and the concentration
{B) and achieved specific activity (a function of R
and F). there seems to be relativelv- little evidence
available for the Dinophyta. However, there are data
on the ratio of chlorophyll a (and other photo-
synthetic pigments) to the reaction centres ot
photoreactions one and two (see Prezelin, 1981;
Dubinski, Falkowski & Wyman, 1986) which suggest
that the Dinophyta are similar to other chrom-
ophytes (Bacillariophyta and Prymnesiophyta) in
this respect. No data seem to be available as to the
ratio of chlorophyll a to other catalysts (e.g. the
cytochrome b,, /complex, or RUBISCO) which are
more likely (on general grounds: Raven, 1984) to
452 jf. A. Raven and R. J. Geider
have an overall rate-restricting R value for photo-
synthesis (and growth) in the Dinophyta (but see
Samuelsson & Prezelin, 1985; Samuelsson ct al.
198.1). Another datum which hears on the ratio of
plastidial catalysts to other catalysts is the ratio of
plastid volume to the volume of the rest of the cell.
Table 2 shows values, based on quantitative electron
microscopy, for the volume of plastid as a fraction of
the volume of the rest of the cell, with the volume
occupied hy e.xtracellular wall (and other) materials,
vacuoles, and polysaccharide storage deposits (starch
in the chloroplasts of members of the Chlorophyta;
starch or a-l,3-glucan outside the two-membrane
portion of the plastid envelope in other divisions)
being excluded. It will be seen that the single
representative of the Dinophyta has a ratio of O32,
while members of other algal divisions represented
range from ()-26 to 0-60; the upper and lower limits
are delined by members of the Chlorophyta and
Dinophyta respectively. Peridininm is thus at the
lower end of the range found for the faster-growing
green algae and diatoms, in general accord with the
notion that Dinophyta ha\e a smaller fraction of
their catalytic volume occupied by photosynthetic
machinery.
Table 2 also gives data on plastid volume as a
fraction of total cell volume uncorrected for these
porticMis of the cell occupied by walls, storage
products or vacuoles. The organisms listed all have
small tractions of the cell volume occupied by cell
walls or vacuoles. The polysaccharide storage in
chlorphyte plastids inflates the plastid fraction of
total cell volume in these cells relative to the other
algal Divisions where the storage polysaccharides are
outside the plastids. On this basis it is clear that the and (jonyattlax polvedra Stein (Meeson & S\veen>',
Dinophyta are at the lower end ol the range, along
with lutf>len(i )>racilis Klebs which also has a lowajJardhii Gom. (Foy, 1983) and Phaeodactyluni
(relative to the fastest-growing members of the
Chlorophyta and Hacillariophyta) specific growth
rate (Raven, 1986, 1987, and references therein).
These data, together with those on photosynthetie
units c|uoted above, permit the tentative conclusion
that one limitation on /^,,, in the Dinophyta might be
a low \aluc of B [ec|uation (1)J, for catalysts of
photosynthesis. This conclusion does not, of course,
rule out a decreased B lor other catalysts downstream
of ph(>tos\nthesis. In view of the 'normal' (for
microalgae) C/N ratio of the dinophytes (Falkowski
('/ al., 1985), and the apparent ahsence of massive .N
reserves in non-catalytic proteins or other forms, we
may reasonably (albeit rhetorically) ask what much
of the N in dinophytes is doing.
!K potential implication of this allocation of
resources in the Dinophyta growing at //,, at the
optimal growth temperature is that it could permit
some offset of the effect of suh-optimal temperatures
on specilic growth rate. This result requires that the
value of B for rate-limiting catalysts (Kacser &
Burns, 1973; Heinrieh et al., 1977; Raven, 1981,
1984o) i.e. those with high F values in equation (1),
is increased, using resources previously unaccounted
for in the analysis of constraints on //, of dinophytes.
Such an outcome would decrease the Q^^.^ of //j,, of
dinophytes (genotypic or phenotypic) to values
lower than those of diatoms or green algae. This
suggestion has two main flaws. One is that there is no
evidence for a lower (3,,, for//,,,, in dinophytes than in
other, faster-growing, micro-algae (e.g. Meeson &
Sweeney, 1982, Thomas, Dodson & Linden, 1973).
niie other flaw, which nature ignores (at least in
ectothermic animals), is that the increased /i \'akie
(or, for an adult determinate-growth animal, in-
creased metabolic activity) at low temperature is
obtained at the expence of //, (or rate of
metabolism) at the optimal temperature. This latter
point has been forcibly made by Hoehaehka &
Somero (1984) in the context of ectothermic animals.
V. Till'. OBSKRVi:n tiFI'-HCTS OF T H M P E R A T U R E
ON KKSOIMU-I-;-LI M ITEl) ALGAL ( i R O W T H
1. Light lirtiitation
There is considerahle variation in the effect of
temperature on specific growth rate under light-
limited conditions and under nutrient-limited
growth.
We deal first with the effect of temperature on
light-limited growth. The ' expeeted' eflect is for
light-limited growth to be much less temperature-
sensitive than is resource-saturated growth (see
section 11). This sort of result is indeeci found in a
number of investigations. I^^xamples are the data on
Ccratiiwt furca (Ehrenherg) Claparode & Lachmann
1982), Oscillatoriti redekei van Cjoor and Oscillatoria
Iricortttitufii (Fawley, 1984).
1 lowever, in other cases the specific growth rate at
limiting photon flux densities is relatively tempera-
ture sensitive; sometimes the light-limited specific
growth rate is as temperature-sensitive as is the
light-saturated growth rate. One example is the
cyanobacterium Microcystis aeruginosa Kutz L'\ -
007 (Kruger & Klofi, 1978) where growth at two
different light-limiting photon flux densities is \ery
temperature-sensitive, albeit not showing 'classical'
exponential increase in // with temperature. While
quotation of a Q^^^ is, then, not appropriate, we note
that an increase in growth temperature from 15 to
25 C causes at least a doubling in the light-limited //.
A further example, and one for which data on
light-limited as well as light-saturated growth are
available, is the diatom Leptocylindrus danictis (Verity,
1982/j). Mere the dependenee on //, and of the initial
slope of the // vs. photon flux density cur\e on
growth temperature are both sigmoidally related to
temperature in the range 5-20 ''C. The Q,,, for //,,
estimated from exponential equations fitted to the
 Temperature and algal growth 453

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454 . A. Raven and R.J. Geider

data, IS 4-4 (5 20 C) and 8-S ( 5 - 1 5 C ) . For temperature for//,,,. At lower temperatures, as Geider
limited growth, the corresponding y,,, values are 3-8 (1987) points out, tbe value ot // at a gi\-en incident
and 4-0 (Verity, 1982/;, p. 212). pboton tlux density is higher. This means tbat the
ratio of catalysts of (temperature independent) light
harvesting and primary photochemistry and of
2. l.itnilation hv chemical resources (temperature independent) downstream thermo-
The effect of temperature on the specilic growth rate chemistry is decreased lor plants growing at lower
i)i' microalf^^ac under nutrient-limited conditions is temperatures. 'Phe changed ratio again can be
less consistent than is that of temperature on light- construed as matching the input of photochemical
limited specilic growth rate. In ^'cneral, it is possible energy to its consumption in growth processes. T b e
to assert that nutrient-limited specific growth rate is acclimatory changes in the ratio of catalysts with
less temperature-dependent than is //, (e.g. for different Q,,, values leads to an increaseci /i value
nitrate-limited growth o'i Dunaliella sp. And (iynmo- (relative to that of organisms with invariant ratios) at
dinium splendens Lebour or SiO.^-limited growth of lower temperatures. However, the changes cannot
Slephanodiscus miiiiitus (irun and Asterionella for- maintain // at the values found at higher teni-
niosa Haas: Thomas & Dodson, 1974; Mechling & perattires, although the difference is much smaller at
Kilham, 1982; Tilman, Mattson & Langer, 1981), low photon t1ux densities.
although this is not always so, at least over the entire However, we have seen (section V) that in a
temperature range studied (e.g. for SiO^^-limited number of cases tbere is a \ ery substantial tempera-
growth of I'halassiosira noidenskioeldii Cleve and ttire effect on tbe light-limited growth rate. We
AslerioneUa forviosti, or phosphate-limited growth concentrate on the data of Verity (1982/;) witb
of the ( yanobactcrium Oscillatoria ai>ardhii Paasche, respect to growth rate of Leptocylindrus danicus.
1975; Ahlgrcn, 1978; Tilman et al. 1981). The Verity (1981fl) had previously shown that rate of
detailed work of Rhec & Cjotham (1981) on Asterio- photosynthesis, measured at the growth tempera-
nella formosa ami Scendesmiis sp. showed that the ture, varied markeclly with growth temperature
elTccts of low temperature and of low concentrations under light-limiting as well as under light-saturated
of N- and P-containing nutrients were more than conditions. When grown under long daylengths
additixc, bi.it where not multiplicative. This is the (15L>:9D, or 12L:92D), P,,,,,,, i.e. the light-saturated
opposite of the first case discussed above, i.e. the pbotosynthetic rate (on a chlorophyll a basis) in-
U-ss-than-additi\'e effects of low temperature and low creased 9-55 fold in the range 5-20 C, while the
concentrations of nutrient solutes. initial slope of the photosynthesis photon Hux density
ctirve (also on a chlorophyll basis) increased 4-1-told
over the same temperature interval. The // \alues
VI. i ; x I M . A N A T I O N O I ' r i l l ' i; I ' I ' i : ( T s o i . - provided by Verity (198^ a) allow conversion of the
| ' I ; M i ' i ; i ! A I I HI-: O N H h : . s ( ) u R C i : - 1 . 1 M I r i u ) A I . ( ; A I . photosynthetic data to a cell C basis for comparison
(; n o W T i l with the data on // in Verity (1982/j). Such conversion
I. Lii;lit limitation to a C basis shows that temperattire effects on
Light limitation of growth in algae is generally photosynthesis are similar to those on growth, and
related to an increased allocation ol resources to that the large temperature dependence of light-
limited specific growth rate is not a function of
pigments and polypeptides related to light harvesting
temperature dependences ol excretion of t:)rganic C
with generally tliminishcd changes in allocation to
(Verity 1981/)) or of dark respiration (Verit\-,
cataKsts of downstream reactions. Phis change m
allocation can be construed as optimising the balance
of the rate of energy sujiply from primary photo- How can the substantial temperature sensiti\ ity of
chemistry and the rate ol energy consumption in ligbt-limited pbotosynthesis (and growth) be ex-
downstream reactions. 'I'his matching has two plained ? The photosynthesis- (and growth-) limiting;
potential advantages. One is that, at low incident processes at low photon Hux densities relate to light
photon Hux tlcnsitics, the conversion of incident absorption and the eHicient transfer of the resultinu
photons into cellular material is increased by the excitation energy to operational and eHicient reaction
higher ratio of light-harvesting pigments to down- centres and downstream reactions. Hoiking these
stream cataKsts in cells acclimated to low photon three partial processes in ttirn, , , the absorption of
Hux densities. 'Phc other potential advantage is that light on a cell C basis is determined by tbe absorptioti
algae acclimated to high photon flux densities, with cross-section (m' mg C '), since a given incident
a lower ratio of light-harvesting pigments to down- pboton Htix density (//mol m " s ') multiplied by the
stream catalysts, should have less tendency to exhibit absorption cross-section yields an absorption rate in
photoinhibition at a given, bigh incident pboton Hux //mol mg C ' s '. Absorption eross-section on a C
density (sec (Jeidcr, 1987). basis IS related to absorption cross-section of chlor-
'Ilic discLission above is implicitly conducted in ophyll c/,,||| (the effective specitic absorption co-
terms of a tcmpcrattirc similar to the optimal elHcient of chlorophyll /// vivo: m~ mg chl a^') \ ia f.
 Temperature and algal grcnvth
We have already seen that light-limited photo-
synthesis, on a chlorophyll a basis, is lower I'or cells
grown at lower temperatures. .A.ccordinKly, if light
absorption l.s the cause of the lowered phofosynthetic
rate, it must be a result of a decrease in c;,. via a
decrease of a,.,,!- ''i <>the'' words, the achieved //; vivo
absorption coefficient is lower in the low-tem-
perature cells. Variations in ,,, reitect changes in
'self-shading' (package eflect), and can be detected
\ ia measurements of / " ?''7.'o absorptance combined
with cell pigment analyses (Osborne & Raven, 1986).
In view of the magnitude of elfects on a,,,,, of a given
increment in cell size, shape or intracellular pigment
distribution (Osborne & Raven, 1986) it is unlikely
that the magnitude of the temperature efTect in
Leptoevlindrus danieiis is a function of a change in
a In anv case, ,.,,| would be expecteci to increase
in cells grown at low temperature due to a reduction
in self-shading consequent on the lower pigment
content.
Excitation energy transfer is an intrinsicalh' more
malleable process than is light absorption. Relatively
minor changes in the arrangement of the various
light-harvesting pigment-protein complexes could
substantially decrease the efficiency ol excitatiorn
energy transfer to reaction centers I rom its achie\-
able value, for high pigment: reaction centre ratios of
greater than 95",,. i^ very high ratio of antenna
pigment to functional reaction centres at low tetnpera-
tures could decrease the chance oi the excitation
energy corresponding to a given photon absorption
e\-ent resulting in photosynthetically useful photo-
cbemistry. Distinction between efficiency of excita-
tion energy transfer per se and the presence of
sufficient effective reaction centres requires measure-
ments of Huorescence, and of the total pig-
ment: reaction centre ratio. 'These measurements,
together with the absorptance measurements men-
tioned earlier, would permit partitioning of the
decrement of photosynthetic efficiency on an in-
cident light basis between the three patial processes
mentioned above. It must be emphasised that, e\en
though the control strength of 'downstream' photo-
SN'nthetic reactions is low at low photon flux
densities, sufficiently large decrements m their
acti\ ity could restrict the rate of photos\ nthesis (see
Kacser & Burns, 197.3; Heinrich el al., 1977).
2. Limitation bv eheniieal resources
Turning to limitation on the supply of chemical
resources, the resource has to mo\'e from the bulk
pbase of the medium to the stirface of the organism
through whatever boundary (unstirrecl) layer is
present, to pass through the membrane by diffusion
through the lipicl part of the membrane, or by
mediated transport in\ol\ing speciHc membrane-
located proteins, and then be assimilated inside the
cell.
455
.'\fter assimilation, the resource participates in
structural, catalytic anci storage components of the
organism. The relation of specific growth rate to
nutrient supply is most immediately expressed in
terms of the internal t]uantity of the ntitrient, i.e. the
cell quota (see Morel, 1987). Specific growth rate is
hyperbolically related to the cell quota of those
nutrients whose concentration is relatively elastic.
These nutrients include N and P, which onK'
contribute 0-1 or less to the dry weight of the
organism. Carbon occupies up to half of the cell dry
weight; accordingly, there is no hyperbolic relation-
ship between cell C c]uota and growth rate. For N
and P growth rate is zero at a Hnite cell (juota (the
minimtim cell quota); increasing cell quota permits
increasing specific growth rate, with decreasing
increments of growth rate with increments of cell
quota tmtil no further increase in growth rate occurs
with increasing cell quota the phenomenon of
' luxur\' accumulation '.
The effect of temperature on ntitrient-linuted
growth rate, considered from a cell C]uota \ iewpomt,
will be consitiereti in terms of the data of Rhee &
(jotham (1981) on the growth of Seenedesnius sp.
under nitrogen and phosphorus-limiting conditions
at a range of temperatures. 'Phe minimum cell (.|uota
for nitrogen and phosphortis increased with de-
creasing growth temperature. 'Phis increase is con-
sistent with a requirement for more nitrogen and
phosphorus at lower temperatures; this effect is more
marked for nitrogen than for |")hosphortis (Rhee tV
(iotham, f98l). In general terms we can account for
this difference between the two elements in terms of
the greater catalytic use of nitrogen than of phos-
phorus. 'Phus a relatively large fraction of cell N is
m catahtic proteins (light-har\ estiiig pigment
protein complexes, soluble cnz\mes/membrane-
associateil transjiorters) and catahtic nucleic acids
rather than structural and storage components; a
rather smaller fraction of cell P ma\' be found m
catalytic nucleic acids, etc. relatix e to structural P in
phospholipids.
'Phe rationale for the argtiment about cell t]uota
antl temperature for cataKtic components is as
follows. Por organisms which are capable of growing,
under optimal resource suppl>' conditions, at specific
growth rates close to the 'theoretical' maximum
considered by Raven (1984(i, f98(), 1987^;; and see
section I\'), the activity of the nitrogen-containing
catalysts in the cells are working at close to their
achievable maximtim rate. .Accordingly, growth
under nitrogen-limiting conditions coLild not in\<)l\ e
substantial increases in the catalytic capacity of
nitrogenous macromolccules. I^^xtending this argu-
ment to changed growth temperatures, substantial
temperature dependence of N-limited growth might
be expected, provided N supply to catalyst synthesis
were not constrained by relatively temperature-
independent transport processes (see abo\e).
456 . A. Raven and R.J. Geider

The temperature dependence of cell synthesis on a would expect that such processes would ha\e
cell N basis can be computed from T\ible 1, and fig, temperature dependences similar to tbose of re-
2 of Rhee & Cotham (1981), The parameter actions catalysed by soluble enzymes (see Stein,
computed is nitrogen use efficiency ot C assimilation 1986), 'ilie situation is of course, potentially com-
in units of mol C assimilated into cell material per plicated hy the possibility o f adaptations ' to tempera-
mol cell N per second, Tbe relatively limited range ture variations by changes in tbe quantity of porter
of cell C content as a lVaetion of cell dry weight in present in unit area of tbe plasmalemma, and/or tbe
microalgae means tbat cbanges in tbe N use eBieiency aliinity of tbe porter for the transported substrate.
in tbe units quoted abo\ e are essentially proportional Increases in eitber or both of tbese parameters would
to tbe value in g dry weight gain per mol cell N per belp offset tbe intrinsic temperature elTect in terms
second. Tbe nitrogen use elficicncies computed Irom of nutrient uptake from growtb-iimiting concen-
tbe data of Rbee & (iotbam (1981) apply to growtb trations of nutrient. An increase in area densitv- of
at a given specific growtb rate (0-5 d ', or ,S-8 x porters at lower temperatures could be accomplished
10 ''s ') at two temperatures (11 and 2(1 C;) witb with a relatively minor reallocation of resources since
tbe growtb rate determined by N sujiply. the piasnialemma proteins are, in sum, a small
The computed efliciencics are 42 //mol C (mol cell traction ol the total cell mass or C, It is important to
N) ' s ' a t 1 1C: and 1 30/miol C (mol cell N)"' s ' at realize that, in whole cell experiments (whetber
20 C, a y,,| value of 3-S, However, it is clear (tigs 1 short-term uptake or long-term growth are measured
and 5 of Rbee & Ciotbam, 1981) tbat 0-5 d"' is close as a tunction ot nutrient concentration) it is not easy
to II at 1 1 C', so tbat changes in // lor increments oi to separate an increased afiinity of the porter from an
cell N c]uota are diminished relative to etfects in cells increase in tbe amount of porter unless tbe in-
growing at O'.S d ' at 20 C, Tbe (->, value is tbus an vestigator bas eliminated tbe possiblity of an excess
overestimate. It is better, where possible, to det- potential at substrate saturation o\'er wbat is ex-
ermine N use etiiciency during growtb at a constant pressed. In practice, we rely bere on estimates of the
fraction of /', at tbe several growtb temperatures. concentration (KJ whicb yields half of the maximum
However, tbis policy is not possible with the data to specific growtb rate at a given temperature. No clear
band. pieture emerges trom investigations of /i tis. nutrient
We tnay , tben, conclude tbat (as expected) tbe cell concentration as a tunction of temperature, Tbus,
t|uota needed to achieve a given N-limited // value is from data obtained by Mechling & Kilbam (1982\
higher at lower temperatures. For organisms wbicb and literature values in Table 1 of tbeir paper, tbere
can maintain a given N cell c|uota, at a range of are three cases in which A.,, increases (i,e, aflinit>
growtb temperatures, a high (P,,, for N-bmited decreases) with growtb temperature, three in which
growtb would be expected. it decreases or goes tbrough a minimum value, and
Tbe data of Rhee & Gotham (1981) permit one 111 which there is nc, clear trend. The extent to
computations of tbe catalytic cOictcncy of I' in RNA which these variations can be attribtited to the
of Scc7U'desnius growtb at difierent temperatures (see difierent nutrients investigated (NO.|~, SiO., and
tbeir tigs 1 and 11). I'Or P-sutficient cells, tbe Q^^^ ot HPO," ), to tbe difTerent culture metbods used
tbe protein syntbesis rate per unit P in RNA is 3-0, (batcb, semi-continuous and cbemostat), and/or to
Tbus for a cell wbicb can maintain a given P cell tbe use ot seven species Irom tour major taxa (tbree
([uota over a range of growtb temperatures, a bigb algal classes, and tbe cyanobacteria) is not clear.
()i,i for P-limited growtb is predicted, More detailed studies are needed before any tirm
conclusions as to general beha\'iour patterns can be
Tbese considerations ot the effects of cell C]uota tor
drawn, especially since these studies do not dis-
N and P on //, lead us to a consideration of factors
tinguish the membrane transport from the unstirred
wbicb alter acquisition ol N and P for cells growing
layer transport steps.
at difierent temperatures.
Diffusion through the boundary layer may exert Transport of some important solutes across tbe
some limitation on tbe rate at which low concen- algal plasmalemma occurs at a significant rate by a
trations ot solutes can he assimilated (see Raven, 'lipid solution' mecbanism. Examples of sucb sol-
1986, I987r) since the temperature etfect on the utes are CO^ (with lipid solution Hux either as tbe
ditiusion of solutes through this boundary layer as sole means ol transport, or, perbaps more commonly,
well as tbe boundary layer tbickness, is smaller tban as a leak in parallel with an inorganic carbon pump)
tbe eflects on the (tbermocbemical) aspects of cell urea (as N source for many microalgae), and glycollic
metabolism, it would be expected that the boundary acid (a re-usable organie excretion product): see
layer limitation would be relatively less important at Raven (1984c;, 1987c7,r), In experiments on giant
lower temperatures. internodal cells of ebaracean algae (Wartiovaara,
Transport across tbe plasmalemma is, for N i l , / , 1942, 1949; see discussion by Stein, 1986), tbe effect
NO, , I1.,PO, /HPO,,- and (in many cases) CO,,/ ol temperature on the 'lipid solution' permeability
HCO., , tbe responsibility of proteinaceous catalysts coefficient of a range of organic compounds is less
(see Raven, 19766, 1980/), 1984fl, 1987r). One marked for the smaller and more lipid-soluble
 Temperature and ali>al
molecules than i'or examples which are hufjer and
less lipid-soluble (Table 1). These experiments
were, howe\'er, carried out o\x'r times which prob-
ablv did not permit ' homeoviscous adaptation' to
the different temperatures vised, so the behaviour oi
lipid-solution permation in cells frenotypically of
phenotypically acclimated to \'arious temperatures is
unclear.
Regardless of the tnechanism ol organic excretion,
it is interesting that Verity (1981 b, 1982/;) found that
the specific excretion rate [mol C (triol Cell C) ' s ']
of Leptocylindrits danieus is independent of growth
temperature. However, the greater surface area per
unit cell C means that the area based flux of organic
C is greater at the lower temperatures.
F o r the assimilation process once the nutrient has
entered the cell, an enzyme is, of course, invoked.
Raven (1976/;, ]9H0b) has argued that transport
(mediated) of solutes such as NO.-, NH,,', \\.,P()^ /
H P O / " , and CO.j/HCO;," into algal cells against a
concentration gradient represents a means of econo-
mizing on resource alloeation to the machinery of
nutrient influx and the initial assimilation process.
Less energy, C and N are, apparently need to
provide, and operate, concentrative transport plus
the assimilation process than would be needed if the
assimilation process had to deal with tiie exogenous
concentration of the nutrient. However, it is not
clear if the concentrative transport process, operating
at low but 'natural' nutrient concentrations, can give
a steady-state concentration of nutrient which satur-
ates the assimilatory enzyme. This is an important
question in terms of the impact ot changes with
temperature in the affinity of the assimilatory
enzyme for its substrate (cf. Hochachka & Somero,
1984). The best data for an algal enzyme eatalysing
the initial biochemical step ol assimilation are for the
carboxylase activity of RUHISCO frorn Larriiiuiria
saccharina (Davidson, 1987). He found that, as with
the higher plant enzyme, the affinity for CO.^
increased with decreasing assay temperature. With
subsaturating external CO.^ concentrations this effect
would, if it applied to the enzyme from plants grown
at different temperatures, help to offset the decreased
substrate-saturated specific reaction rate of the
enzyme at the lower temperatures and help to
maintain the rate of assimilation per unit enzyme as
temperature is decreased. Furthermore, Daxison &
r3a\-ison (1987) found a greater substrate-saturated
carboxylase activity (on a fresh weight basis) of
Larninaria saccharina RUBISCO in thalli acclimated
to lower temperatures.
For an organism with difiusi\e entry of C()^ the
above mentioned temperature ellects on the kinetics
of Latniuaria saccharnia might be aided in main-
taining the rate of photosynthesis at lower tempera-
tures in air-equilibrated sea water by the increased
CO., solubility and, in terms of the carboxy-
lase: oxygenase aeti\ity ratio of RL'HISCO, the
457
higher ratio of CO.^ solubility to O. solubility, at low
temperatures. I lowexer, the significance ol this is
obscured by the probable occurrence ol a COo
concentrating mechanism in this alga (Iverb\' &
Raven, 1985).
Data from micro-algae also bear on the extent to
which RL'BISCO acti\ ity may be related to tempera-
ture effects on photosynthesis and growth. Li &
Morris (1 982) give data on the diatom Phaeodactylum
tricarnutuni which relate growth temperature to
specific growth rate, specific photos> nthetic rate,
and the speeific acti\'ity of the carboxylases RI H-
ISCO and I'RPcase, all presented as pg C incor-
porated (pg cell C)"' day''. The data relate photo-
synthesis at both the growth temjierature and the
optimal temperature for photosynthesis to the speci-
fic growth rate at a gi\en temperature. The carboxy-
lase data are gi\en as the activity at the optimum
temperature for the carboxylase for extracts of algae
grown at each experimental temperature; from the
activation energy data provided it is possible to
compute the specific reaction rate at the growth
temperature. The RUBISCO data show that the
activity at the optimal temperature of 40 C, and on
a cell C basis, increased with a decrease in growth
temperature in the range 25 10 C, with a decrease
on a further lowering to 5 C. These changes were
interpretted b\- Li & Morris (1 982) as a conipensation
phenomenon (see section II), i.e. more RL'BISCO
activity per unit cell C at lower temperatures.
How e\ er, it is not immediately ob\ ious that compen-
sation is \ ery effective in I^haeodactytuni tricoruutum.
The Q,|, of RUBISCO from this organism is 21 (Li
& Moi'ris, 1982), and the increase in enzyme acti\it>'
per cell C" at the temperature optimum is 2'5-fold
over the range 25 15C, so that the RIU5ISCO
activity at the growth temperature is 1-2-fold higher
for 15 C cultures than for 25 C cultures. Howe\'er,
//, decreases 1-2-fbld (\'ia the maximum at 20 C)
over this range. Furtherniore, over the range 15 5 C ,
/', decreases more than 3-5-fold, while photo-
synthesis deereases 2-6-fold, and Rl'BISCO activity
decreases 2-3-fold. ()\er the intermediate range
20-10 C, //, decreases 2-4-fold, while RUBISCO
activity decreases 1-2-fold. Compensation is most
marked near the temperature optimum for growth,
while compensation is inverse at lower temperatures.
The data of Li & Morris (1982) do not support the
view that RUBISCO is present in large excess of that
needed to account for photosynthesis; the activities
reported are inadequate (when corrected from the
temperature optimum to the growth temperature) to
account for the observed rate of photosynthesis.
As with the Laniiiiaria saccharina data discussed
earlier, interpretation in terms of restriction ot
photosynthesis by CO., transport relative to that by
RUBISCO activity under natural conditions is
complicated by the likelihood that Phaeodactylum
tricornutuni has a CO., concentrating mechanism
458 J. A. Raven and R.jf. Geider
(Burns & Beardall, 1987; cf. Patcl & Merrctt,
1986).
Data from microalgae are also available for natural,
multispecics marine populations (Li et al., 1984;
Smith & Platt, 198.S). These studies show a greater
response of RUBISCO activity to temperature in
arctic than in tropical phytoplankton. Further, it
appears that the arctic populations do not apparently
respond to a lower temperature by an increase in
RL'BISCC) activity per unit photosynthetic pigment,
although interpretation of data from natural popu-
lations may well be confounded by variation in, for
example, nutrient availability.
In attempting to draw conclusions as to the role ot
resource reallocation in accounting for the Q^ ot
nutrient-limited micro-algal growth we are, ol
course, faced with the problem of variability in the
phenomenon to be explained (section V above), i.e. a
decrease in the (P,,, of /J as a result of nutrient
limitation for some genotypes, but little etieet in
others. I'^or planktonic microalgae the dependence of
//,,, on cell size (/(, smaller for larger-celled geno-
types) is less than that for the impediment to
dilVusion to the cell surface through unstirred layer
(greater impediment for larger cells): see Raven
(1986, 1987r). Other things being equal, diffusion
through unstirred layers is more likely to limit
nutrient-limited growth in larger-celled microalgae.
Since the C-'io "^ dilTusion of nutrients in aqueous
solution is lower than that of the great majority of
catalysed cellular process (Table I), we might expect
larger cells to have a less temperature-dependent /i
under nutrient-limited conditions than would smal-
ler cells il' diffusion through the unstirred layer were
a significant constraint on nutrient-limited //. This is
not obviously so for the examples quoted in section
V. There is thus little ground for attributing the
examples of low nutrient-limited O,,, values for
growth (section V) to limitation by diffusion through
unstirred (boundary) layers, especially in view of the
general (not specilically related to temperature)
considerations of Ra\'en (1986, 1987r). Application
of analyses of the kind suggested by Morel (1987)
shoLild prose useful here.
VII. CONCI.llSIONS
The discussion herein attempts to interj^ret the
elTects of suboptimal temperatures on algal growth
in terms of three tactors. One concerns the intrinsic
effects of temperature on catalysts ot biochemistry or
transport, on transport barriers and on structures. A
second concerns changes in the properties of eata-
lysts, barriers and structures such that, for example,
an en/.yme is replaced in an organism growing at a
lower temperature by an isoform with properties
which are more appropriate to the lower tempera-
ture, or membrane hpid composition is changed to
keep lipid viscosity constant. The third relates to
ehanges in allocation of resources between, or within,
catalysts, barriers, structures and stores.
From data discussed elsewhere (Ra\'en, 1984rt,
1986, 1987c/) it would seem that, at //,, the fastest-
growing microalgae are close to the //, permitted by
the intrinsic capacity of their catalysts, the dictates of
metabolic regulation, and need for structural and
storage materials. Decrease in temperature bas one
widespread response. The ratio of catalysts dealing
with steps of photosynthesis from light absorption
through to primary photochemistry, i.e. those which
are temperature-insensitive, to those of downstream,
temperature-sensitive reactions, is decreased. This
decrease appears to bring these two steps into balance
and may also serve to oflset photoinhibition. Any
substitution of catalysts as a response to temperature
change is not well documented for microalgae.
Where the analysis of resource allocation and
properties of catalysts tails down is in explaining,
mechanistically, why some organisms ha\'e intrinsic-
ally low //, values at their temperature optimum, and
do not show a decreased Q^^ of // at suboptimal
temperatures.
For growth in suboptimal resource supply condi-
tions the analysis of resource allocation and intrinsic
catalytic capacities and kinetics gives a satisfactor\'
explanation ot the low Q,,, for // under light-limited
conditions. Explanation of the low (P,,, for /( under
nutrient-limited conditions is less certain.
A f K N O W L !; U C; F. M ! N T S
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