FEMS Microbiology Ecology, 94, 2018, fiy175

doi: 10.1093/femsec/fiy175
Advance Access Publication Date: 30 August 2018
Minireview

MINIREVIEW

The role of wetland microorganisms in plant-litter

decomposition and soil organic matter formation: a

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critical review
Stephanie A. Yarwood*
Environmental Science and Technology Department, University of Maryland, 1204 HJ Patterson Hall, College
Park, MD 20742, USA
∗
Corresponding author: Stephanie A. Yarwood, Environmental Science and Technology Department, University of Maryland, 1204 HJ Patterson Hall,
College Park, MD 20742, USA. Tel: +1 301-405-1345; E-mail: syarwood@umd.edu
One sentence summary: Review of recent wetland microbiology focused wetland soil organic matter formation.
Editor: Marcus Horn

ABSTRACT
New soil organic matter (SOM) models highlight the role of microorganisms in plant litter decomposition and storage of
microbial-derived carbon (C) molecules. Wetlands store more C per unit area than any other ecosystem, but SOM storage
mechanisms such as aggregation and metal complexes are mostly untested in wetlands. This review discusses what is
currently known about the role of microorganisms in SOM formation and C sequestrations, as well as, measures of
microbial communities as they relate to wetland C cycling. Studies within the last decade have yielded new insights about
microbial communities. For example, microbial communities appear to be adapted to short-term fluctuations in saturation
and redox and researchers have observed synergistic pairings that in some cases run counter to thermodynamic theory.
Significant knowledge gaps yet to be filled include: (i) What controls microbial access to and decomposition of plant litter
and SOM? (ii) How does microbial community structure shape C fate, across different wetland types? (iii) What types of
plant and microbial molecules contribute to SOM accumulation? Studies examining the active microbial community
directly or that utilize multi-pronged approaches are shedding new light on microbial functional potential, however, and
promise to improve wetland C models in the near future.

Keywords: soil organic matter; microbial plasticity; functional redundancy; metabolic diversity; plant decomposition

WETLAND SOIL ORGANIC MATTER
FORMATION
The destruction of one hectare of coastal wetland has an esti-
mated carbon (C) loss equivalent to 10–40 hectare of temper-
ate forest (Mcleod et al. 2011; Macreadie et al. 2017a). Although
the RAMSAR convention (Ramsar.org) and other international
efforts have helped to underscore their importance, wetlands
are still being lost. For example, across the globe tidal wetlands
are lost at a rate of 1.5% annually (Pendleton et al. 2012), due both
to anthropogenic disturbance and sea level rise (Kassakian et al.
2017). In spite of their C sequestration potential, most restored
or created wetlands are designed to improve water quality or
to provide wildlife habitat. C sequestration may soon become a
more common goal, however, as countries and regions consider
cap-and-trade strategies to limit C emissions (Macreadie et al.
2017b). Unfortunately, restored wetlands tend not to accumu-
late C, even decades after establishment (Ballantine and Schnei-
der 2009; Moreno-Mateos et al. 2012). Moreno-Mateos et al. (2012)
compared 103 wetlands of different types and restoration ages.
They reported that C storage remained 23% lower on average
compared to reference wetlands of the same types. Wetlands

Received: 12 November 2017; Accepted: 29 August 2018


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 2 FEMS Microbiology Ecology 2018, Vol. 94, No. 11
that were slowest to accumulate C were found in cold regions
and were smaller in total area. Moreno-Mateos et al. (2012) also
reported that depressional wetlands were slower to recover than
riverine and tidal influenced sites, but Yu et al. (2017) examining
48 restored sites reported that depressional wetlands recovered
faster than riverine wetlands. This discrepancy underscores that
current knowledge is lacking on conditions and mechanisms
that lead to C storage in wetlands. Soil microorganisms are inte-
gral in plant decomposition and soil organic matter (SOM) for-
mation, and knowledge of these communities is needed for pre-
dictive understanding of wetlands and other soil ecosystems
(Bardgett, Freeman and Ostle 2008).
Studies designed to examine wetland C cycling have often
focused on biogeochemistry (Kayranli et al. 2010), assessing wet-
lands from the perspective of total inputs and outputs to deter-
mine if they are sinks or sources for C (Wynn and Liehr 2001).
These kinds of studies have revealed considerable variation in
C cycling across wetland types. For example, Bernal and Mitsch
(2012) reported that depressional wetlands sequestered signif-
icantly more C compared to riverine wetlands in Ohio, USA.
Reviewing literature world-wide, Kayranli et al. (2010) concluded
that natural wetlands have a higher C sequestration potential
than constructed wetlands, and that restored wetlands are ini-
tially a source for C and that it might take decades for them to
become sinks. They further advised that after reviewing the lit-
erature, more research was needed on the impact that temper-
ature, oxygen penetration and water column fluctuation had on
microbial C turnover.
Until recently, microorganisms were not specifically studied
in relationship to SOM formation. This was due in part to a
wide-spread belief that stored C remains primarily in the form
of undecomposed plant litter, in contrast to microbial-derived
molecules (Brinson, Lugo and Brown 1981; Keddy 2010). Plants
compounds such as lignin were thought to be particularly recal-
citrant. This view has been changing for several years, how-
ever, as new methods of SOM characterization has increasingly
identified microbial residues within stable SOM (Kögel-Knabner
2017). Several studies have demonstrated that lignin turnover
may be slower than cellulose but that it still degrades on the
order of years (Lützow et al. 2006; Rasse et al. 2006; McKee et al.
2016) although similar studies are still needed for wetlands.
Liang and Balser (2008) observed significant microbial-derived
amino-sugars in glacial till soils, including subsurface soils that
were seasonally flooded, and Miltner et al. (2012) visualized cell
well residues attached to mineral particles in an upland soil
and on sterile media incubated with groundwater. Some studies
have shown that SOM composition is dependent both on plant
inputs and the soil microbial community (Grandy et al. 2009;
Schmidt et al. 2011), and it has been hypothesized that microbial-
derived products may preferentially be stored within aggregates
and on mineral surfaces (Cotrufo et al. 2013; Liang, Schimel and
Jastrow 2017), sometimes referred to as ‘protected’ SOM.
Contrasting upland soils to wetlands, anaerobiosis has
thought to be the most significant factor controlling C fate.
The enzymatic ‘latch’ hypothesis posits that anaerobic condi-
tions prevent decomposition by inhibiting oxidase and hydro-
lase enzymes (Freeman, Ostle and Kang 2001). Research in
peatlands across a wide-latitude gradient supports this mech-
anism (Pinsonneault, Moore and Roulet 2016), but it has been
called into question in tropical soils where O2 availability and
hydrolytic enzyme activity did not correlate (Hall, Treffkorn and
Silver 2014). The enzymatic latch may not hold true in restored
wetlands, that are mineral, where C accumulation is lacking
even when plant primary productivity is high and sufficient
flooding conditions are achieved (Yu et al. 2017). In restored wet-
lands, C may be subject to considerable decomposition even
under anaerobic conditions or alternatively aerobic decomposi-
tion is still prevalent in spite of hydrology. Across different wet-
land types and locations both mechanisms are likely at work.
Recent research suggests that variations within microbial func-
tional guilds can contribute to differences in wetland C cycling
rates (Hunger, Gößner and Drake 2015), but the impact of micro-
bial composition on decomposition rate and C fate is the least
understood component of wetland biogeochemistry.
In a recent review, Neori and Agami (2017) pointed out that
there was not enough literature in the mid-1990s to write a
review on wetland rhizosphere microorganism, and in fact few
reviews exist before the early 2000s. One of the first reviews
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described functional groups, but largely concluded that research
was sparse on many aspects of wetland microbiology (e.g. myc-
orrhizae, environmental controls on microbial communities and
plant–microbe interactions) (Gutknecht, Goodman and Balser
2006). However, the last decade has seen a substantial increase
in interest surrounding these topics. The current review is a syn-
opsis of wetland soil microbiology with a particular focus on
the role of microorganisms in plant litter decomposition and
SOM formation. However, there have been a number of other
reviews that have addressed other aspects of wetland microbiol-
ogy. Some of these reviews are described here to provide further
resources for readers beyond the scope of this publication. Neori
and Agami (2017) provides general descriptions of the wetland
rhizosphere biota that includes viruses, bacteria, fungi, proto-
zoa, nematodes and invertebrates, and should be accessed par-
ticularly for information concerning groups not covered here.
Lamers et al. (2012) also focused on rhizosphere microbial com-
munities but did so with the purpose of describing the vari-
ous ways that microorganisms could influence plant growth and
vegetation composition. Their review described the influence of
microbes on pH, nutrient availability, toxicity and oxygen avail-
ability that can influence wetland plants. The role of microor-
ganism both in contributing to the formation of and remediat-
ing toxic compounds such as heavy metals has been the focus
of many studies and reviewed recently (Karimian, Johnston and
Burton 2018), therefore this review will contain limited descrip-
tions of toxins. Similarly, there are two excellent reviews focused
on microorganisms in treatment wetlands (Faulwetter et al. 2009;
Weber 2016), and readers are directed to those article for specific
discussion of different types of systems and the application of
molecular tools there.
This review first addresses how mechanisms for SOM for-
mation may differ in wetlands soils compared to upland soils
where most SOM research has been conducted. This descrip-
tion includes microbial characteristics unique to saturated sys-
tems (e.g. anaerobic metabolism, interactions with metals and
dynamic shifts in redox) and compares conditions across dif-
ferent wetland types (e.g. temporal salt marshes, tidal freshwa-
ter wetlands, peatlands and depressional wetlands). Given the
assumed importance of microbial composition in forming SOM,
the review then synthesizes publications that use high through-
put sequencing to examine bacterial communities with the goal
of identifying dominant taxa and reconciling observed composi-
tion patterns with potential metabolic capacity. Here the discus-
sion includes the limitations associated with sequence charac-
terization and demonstrates how microbial plasticity and func-
tional redundancy can hamper efforts to link structure and func-
tion. The review concludes by identifying knowledge between
wetland microorganisms, decomposition and SOM storage. Here
publications using multi-pronged approaches such as isotopes,

enzyme assays and SOM characterization will be included; as
will suggestions for future investigations.
WETLAND PROPERTIES THAT SHAPE CARBON
FATE
Wetland hydroperiod and soil redox
The term wetland encompasses ecosystems, having a wide
variety of soil conditions driven primarily by hydrology, which
results from the balance between surface and subsurface water
inflows and outflows and evapotranspiration. Wetlands can
develop hydric soils if continuously saturated for a few weeks
a year during the growing season, and at the other extreme soils
are permanently flooded. The variation of flooding frequency
within and between individual wetlands can translate to dif-
ferences in microbial communities, but clear patterns are diffi-
cult to observe. In a study comparing created wetlands that dif-
fered in hydrologic regimes, soil bacterial composition differed
between treatments and more diversity was observed in drier
compared to wetter wetland sites (Ahn and Peralta 2009). In con-
trast, a laboratory study that imposed different levels of flood-
ing frequencies also observed differences in composition but
reported an increase in diversity under more saturated condi-
tions (Randle-Boggis, Ashton and Helgason 2018). Furthermore,
when Yu and Ehrenfeld (2010) compared wetlands along a soil
catena, they found differences between microbial composition
of wetter cedar swamps compared to drier maple swamps and
pine wetlands, but did not detect differences in diversity.
The relationship between hydrology, redox state and micro-
bial community composition is influenced by several confound-
ing variables. One significant complications is the role of plant
radial O2 leakage which can increase soil redox state indepen-
dent of water level. The extent to which plants supply O2 to
their roots varies greatly between and within species (Voesenek
et al. 2006; Lai et al. 2011). In temperate marshes, species such
as Phragmites australis (common reed) and Typha spp. (cattails)
(Grosse, Armstrong and Armstrong 1996) have pressurized roots
and comparatively higher ventilation efficiency compared to
plants like Peltandra virginica (Arrow arum) where roots are only
aerated via passive diffusion (Frye, Mills and Odum 1994). Within
species, the Eurasian lineage of P. australis (Cav.) Trin. ex Steud.
subsp. australis, has a ventilation efficiency 300% greater than
the North American P. australis subsp. americanus lineage (Tul-
bure et al. 2012). Plant radial oxygen leakage can also influence
C cycling in cold peat bogs, as was demonstrated in Patagonia
by comparing methane (CH4 ) emissions and redox potential in
Sphagnum systems with and without cushion plants (Astelia spp.
and Donatia spp.) (Fritz et al. 2011). Here the vascular plants cre-
ated extensive root systems, and the authors observed increased
soil aeration and decreased CH4 emissions.
Water level and radial O2 leakage can vary daily (Faußer
et al. 2016) and seasonally (Neubauer et al. 2005), leading to con-
stantly changing conditions for the soil microbial community.
Interestingly, microbial communities may be adapted to these
fluctuating conditions and therefore, remain stable over time.
DeAngelis et al. (2010) demonstrated that when tropical forest
soils were placed under constant anaerobic or aerobic condi-
tions microbial composition changed over the course of the 4-
day incubation, but that microbial composition did not change
when redox potential was cycled between aerobic and anaero-
bic conditions. Similar findings were reported for constructed
wetland soils (Peralta et al. 2014). In another constructed wet-
land system, microbial community composition did not change
Yarwood 3
when hydroperiod was varied over the course of several weeks
to simulate storm events, even though increased denitrifica-
tion rates were noted when soils were wetter (Ishida, Kelly and
Gray 2006). Similar stability in methanogen community com-
position was reported in rice paddies (Yuan, Conrad and Lu
2009). Microbial community composition also did not change
seasonally in floodplain soils (Moche et al. 2015) or peatlands
(Sundh, Nilsson and Borga 1997). Within boreal mires, Juottonen
et al. (2008) reported minimal seasonal variation in methanogen
composition using DNA-based T-RFLPs, but found good agree-
ment between increased CH4 flux and increased mcrA (methane
co-enzyme A) mRNA abundance in the winter. Adaptation to
dynamic conditions creates logistical issues for researchers
wanting to study microbial communities in the lab and should
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be considered before creating aerobic or anaerobic microcosm
conditions.
The reduction and oxidation of metals
Hydrology and radial O2 leakage drive differences in the oxida-
tion state of metals and therefore site minerology interacts with
hydrology to shape the wetland microbial community. For exam-
ple, wetland roots are often coated with iron (Fe) (III) and Man-
ganese (Mn) (IV) oxides (Yang, Liu and Ye 2012) (Fig. 1). Plants
supply electron donors in the form of root exudates and oxi-
dize metals through O2 leakage, supporting metal-reducing bac-
teria (Fig. 2). As a result, in mineral wetlands, Fe(III)-reduction
appears to be a major sink for C (Thamdrup 2000; Neubauer
et al. 2005; Sutton-Grier and Megonigal 2011). A review exam-
ining the effects of plants and microbial processes on CH4 emis-
sions concluded that N inputs have little effect on C fate, even in
treatment wetlands receiving large N inputs (Laanbroek 2010).
Especially in temperate wetlands, plants take up considerable
N leaving little mineral N available and resulting in little com-
petition between denitrifying communities and methanogens.
In contrast, both Mn (IV) and Fe (III) oxides can be common in
mineral wetlands, such as those formed in temperate riverine
systems. There is considerable overlap between microbial iso-
lates able to reduce Mn (IV) and Fe (III) (Poole 2004), although Fe
(III)-reduction has been investigated in more detail.
Metal reduction depends on the local crystal structure of Fe
(III) or Mn (IV) and the form of available C. In the rhizosphere,
newly oxidized Fe (III) is primarily crystalline ferrihydrite that
is readily available for Fe (III)-reducers. Geobacter spp., the first
identified wetland Fe (III)-reducers, primarily use acetate as an
electron donor and reduce ferrihydrite (Lovley and Phillips 1987).
However, Geobacter spp. do not efficiently reduce crystalline Fe
(III) such as goethite or hematite (Fig. 2). Recent research has
shown that in addition to Geobacter spp., wetlands can contain
a variety of metal reducers, including those that reduce crys-
talline Fe (III) forms and that can use other C sources (Hori et al.
2010; Lentini, Wankel and Hansel 2012). Lentini, Wankel and
Hansel (2012) observed that when acetate was used in enrich-
ments from the edge of a freshwater pond, Geobacter spp. was
most abundant, but the community shifted when supplied with
glucose and lactate. Similarly, cultured Mn (IV)-reducers have
also been observed to use fermentation products such as succi-
nate and acetate (Myers and Nealson 1988). Most culture-based
studies supply metal reducers with simple compounds, mean-
ing there is little information on the substrates that metal reduc-
ers might use in situ.However, metal reducers may be dependent
on and metabolically linked to fermenters that produce sim-
ple compounds (Bongoua-Devisme et al. 2013). Using lab incu-
bations of tropical rice paddy soil, Bongoua-Devisme et al. (2013)
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Figure 1. Beginning with above- and below- ground plant inputs, the figure illustrates the various transformations of C mediated by the wetland microbial community.
The left side of figure shows how plant materials, such as cellobiose, are processed by the anaerobic microbial community into primary and secondary fermentation
products that can be used by microorganisms as alternative electron acceptors. The insert illustrates processes within the rhizosphere, particularly those linked to
metal cycling, which may be a key C storage mechanism.

reported that Fe(III) reduction was carried out by a diverse com-
munity of facultative anaerobic and anaerobic bacteria some
of which used C directly and others that are known to use H2 .
The Fe (III)-reducers may also use particulate SOM as an elec-
tron shuttle, rather than as a substrate—a unique SOM oxida-
tion process observed first in freshwater riparian wetland soils
from Alabama, USA (Roden et al. 2010).
The frequent transformations of metals between their oxi-
dized and reduced states may play a direct role in C storage.
Organo-mineral complexes are known to contribute to C sta-
bilization with an estimated capacity of ∼1 mg C m−2 of min-
eral surface (Keil et al. 1994). Across multiple soil and sediment
types, SOM binding is highest in materials that contain Fe (III)/Al
oxides (O’Rourke et al. 2015) with poorly crystalline structure
(Bachmann et al. 2008; Lalonde et al. 2012). Lalonde et al. (2012)
estimated that 20% of C in marine sediments is Fe-oxide bound.
One of the defining characteristics of mineral wetland soils is the
presence of redoximorphic features that include nodules and
concretions of precipitated Fe(III) and Mn(IV) (Hickey, McDaniel
and Strawn 2008), and organic C has been observed in the center
of some nodules (Wilson et al. 2013). Given the possibility of co-
precipitation of C with metals, both rhizosphere C and microor-
ganisms that are closely linked to metal transformations may
be important in storing SOM. However, the long-term stability
of this C is not clear. Huang and Hall (2017) demonstrated that
increased flooding during restoration of agricultural site back
to wetlands could increase metal reduction and subsequently
increase C availability. A similar fate could be true for soils inun-
dated due to sea level rise, but this mechanism needs further
investigation.
The wetland rhizosphere effect
Besides radial oxygen leakage, wetland plants can shape the
microbial community through differences in root exudates.

Figure 2. The thermodynamic ladder shows the Gibbs free energy (Gr o ) under standard conditions (25◦ C and 0.1 MPa) expressed as kilojoules (KJ) per electron (e− )
transferred for common electron donors and acceptors in wetlands. Values are taken from (Arndt et al. 2013).
Comparing the root zones of four plant types in tidal freshwa-
ter wetlands, Prasse, Baldwin and Yarwood (2015) observed dif-
ference in the bacterial and archaeal community composition
between plant species in natural wetlands but not in restored
wetlands. There are a wide variety of published results assess-
ing differences in microbial functions between wetlands of the
same type and within a similar geographic area. Hopfensperger
et al. (2009) measured denitrification across tidal freshwater wet-
lands, but did not observe difference in denitrification poten-
tial between different wetland elevations or plant communities.
Ström, Mastepanov and Christensen (2005) collected soil mono-
liths from a single peat bog in Southern Sweden and measured
CH4 flux from different monoliths supporting the growth of
three different plant species. They found that soils under Carex
rostrata emitted more CH4 compared to Eriophorum vaginatum
or Juncus effuses. Similar difference in CH4 emissions between
plant types were observed in another freshwater mescosm study
(Andrews et al. 2013). Both sets of authors reasoned that differ-
ence in plant root exudates contributed to difference in CH4 flux,
but neither explicitly measured them.
Root exudates provide a ready supply of low molecular
weight molecules that can drive methanogenesis (Koelbener
et al. 2010) and other wetland functions. Chen et al. (2016)
characterized roots exudates between four wetland plants and
observed differences in compounds that correlated to differ-
ences in the rhizosphere microbial community. In spite of radial
O2 leakage that increases redox, CH4 production tends to be
higher in vegetated wetlands (McNicol et al. 2017), presumably
due to increased C inputs. The differences in C compounds
between plant species could impact methanogensis through a
number of different pathways. Hydrogenotrophic methanogens
not only access H2 via secondary fermentation, but formate can
be released from plant roots and easily degraded to H2 , bypass-
ing multiple fermentation steps (Hunger et al. 2016; Schink et al.
Yarwood 5
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2017). The conversion of formate to H2 is likely mediated by
a diverse group of facultative aerobic organisms (Hunger et al.
2016), although no studies have specifically targeted this group
for characterization. The central role of formate in driving rhi-
zosphere metabolism has only recently been recognized, and it
remains to be determined what impact this has on total ecosys-
tem CH4 flux and C fate (Hunger et al. 2016).
Mixed-species biofilms can form within the rhizosphere, cre-
ating opportunities for C exchange and competition between
microbial functional groups. Rhizosphere soils supporting
methanogens also contain metal reducers that compete for
the same substrates and methanotrophs that consume CH4 .
Biofilms from Typha latifolia and P. australis roots were found to
contain large numbers of CH4 -oxidizing bacteria (34–43% of the
total community) (Faußer et al. 2012). Population size of CH4 -
oxidizers was also observed to vary between wetland species
and are likely a significant determinant of CH4 emissions across
wetland types (Ström, Mastepanov and Christensen 2005).
Although sometimes overlooked in wetlands, mycorrhizal
fungi have been observed in many wetlands locations and are
also a possible sink for root exudates. A recent review iden-
tified approximately 100 different wetland plant species that
have been shown to host arbuscular mycorrhizal (AM) fungi,
spanning numerous wetland types (Xu et al. 2016, references
within). AM colonization is greatest in drier wetland areas com-
pared to waterlogged locations (Miller and Bever 1999) and drier
locations appear to support increased diversity (Wirsel 2004).
AM fungi seem to consistently alter plant C partitioning in
favor of increased root biomass (Miller and Bever 1999; Stevens,
Spender and Peterson 2002), but other plant physiological effects
remain unknown. For example, AM fungi are often associated
with increased phosphorus (P) uptake in uplands, but results are
 6 FEMS Microbiology Ecology 2018, Vol. 94, No. 11
mixed for wetland species. One study examining Lythrum sali-
caria L. (purple loosestrife) in temperate marshes did not detect
any nutritional benefit of AM colonization (Stevens, Spender
and Peterson 2002), but another study using Kandelia obovata
seedlings (a type of mangrove) in tropical wetlands observed
enhanced P uptake when plants were inoculated with AM fungi
(Xie et al. 2014). These contrasting results suggest that more
research is needed to understand how plant species and AM
composition impact functional attributes. Even less is known
about ectomycorrhizae in wetlands, such as peatlands (Thor-
mann 2006) and swamps (Asemaninejad, Thorn and Lindo 2017),
including the amount of plant C they assimilate. In fact, the rel-
ative contribution of root exudates compared to plant structural
components to SOM-C is not known for wetlands.
Plant litter decomposition
In upland systems, decomposition of plant material typically
begins with colonization by aerobic soil fungi, some of which
produce large quantities of extracellular cellulases and ligni-
nases (Sánchez 2009). As was alluded to earlier, one proposed
mechanism for wetland C storage has been a lack of these
enzymes due to anaerobic conditions (Freeman, Ostle and Kang
2001). Due to the focus on anaerobiosis, fungi have historically
been considered to play a minor role in wetland plant decom-
position (Khan 2004). Saprobic fungi could take advantage of O2
in the rhizosphere, but appear to be most abundant in standing
plant biomass and recently collapsed plant litter (Kuehn 2016)
(Fig. 2). Kuehn et al. (2011) tracked extensive fungal coloniza-
tion of standing dead Typha biomass in temperate freshwater
marshes and calculated that 22% of the plant C was converted
to fungal biomass over the course of one year. This preprocess-
ing of plant litter before it enters wetland soil is an important,
albeit often overlooked, step that allows for extensive fungal col-
onization and the decomposition of plant cellulose and lignin.
Examining stands of P. australis in Swiss marshes, researchers
observed that fungi continue to contribute to decomposition
(0.2–2.4 mg C m−2 day−1 ) after plant materials fell to the soil sur-
face, but at that point bacterial colonization resulted in a much
higher decomposition rate (2.6–18.8 mg C m−2 day−1 ) (Buesing
and Gessner 2006). A review of peatland microbial communities
suggested that saprobic fungal composition is most influenced
by plant litter type and differs between fens and bogs (Ander-
sen, Chapman and Artz 2013); one study found fungal isolates
varied considerably with fens having more fungal diversity and
only sharing 19% species similarity to bogs (Trinder, Johnson and
Artz 2008).
Although fungi degrade lignin and hemicellulose at faster
rates, bacterial ligninases and cellulases are also common
(Burns et al. 2013). The role of bacterial lignin degradation has
not been extensively studied (Bugg et al. 2011) and there do not
appear to be any studies of this process in wetlands. Bacte-
rial cellulases, on the other hand, were recently identified using
shotgun metagenomics applied to estuary soils from North Car-
olina, USA. Several bacterial phyla contained cellulose degrada-
tion pathways: Chloroflexi, Bacteroidetes, Gemmatimonadetes, Planc-
tomycetes, WOR-1 and WOR-2 (Baker et al. 2015). Using 13 C
labelled cellobiose, another group of researchers tracked C into
members of the Firmicutes, Proteobacteria, Acidobacteria and Ver-
rucomicrobia within Finnish boreal fens (Juottonen et al. 2017).
The bacteria able to decompose cellobiose are estimated to be
twice as numerous as the bacteria able to degrade both poly-
meric and monomeric cellulose (Berlemont and Martiny 2013).
A likely scenario is that aerobic fungi begin the decomposition
process while plant litter is standing, contributing to depoly-
merization of plant structural components. Following collapse
of the litter, facultative anaerobic bacteria colonize. These bac-
teria are capable not only of breaking down cellobiose but of fer-
mentation, producing acetate, H2 and other byproducts (Fig. 1).
In support of this model, two studies (Baker et al. 2015; Juot-
tonen et al. 2017) identified cellobiose-degrading bacteria that
were also capable of fermentation, and these findings are con-
sistent with other metagenomic findings in an anaerobic aquifer
(Wrighton et al. 2014). Overall this lends support for conversion
of plant C to microbial biomass, but does not completely exclude
the storage of plant compounds as SOM.
When comparing decomposition of two freshwater marsh
plants Eleocharis cellulosa (spike rush) to Cladium jamaicense (saw
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grass), E. cellulosa decomposed at a faster rate likely due to a
lower C:N ratio and both plants had a faster decomposition rate
at a site within the Florida Everglades, USA, that had more sat-
urated soil conditions (Pisani et al. 2018). This effect of hydrol-
ogy on decomposition was counterintuitive but speculated to
be the result of dry summer conditions that resulted in dif-
fusion limited conditions. Regardless of plant species, roots
and rhizomes decomposed slower compared to above ground
plant parts (Pisani et al. 2018) and contained relatively resis-
tant suberin and polyphenolic lignin. Another study examining
C complexed on mineral surfaces from upland soils reported the
presence of plant lipids, lignin derivatives and suberin (Angst
et al. 2017). These studies suggest that plant root materials are
likely to be stored preferentially compared to other plant parts.
The connection between these types of root-derived compounds
and metal plaques as a mechanism for C storage has not been
reported in the literature but is an exciting area for future inves-
tigation.
The ability of microorganisms to access stored SOM follow-
ing the addition of fresh labile C has been discussed in many
soil ecosystems. Often referred to as a ‘priming effect’ relatively
more bioavailable compounds such as plant root exudates can
stimulate the microbial community and lead to increased C min-
eralization and a decrease in SOM (Zhu et al. 2014). Increased
atmospheric CO2 could lead to more root exudates but trigger
loss of SOM (Bridgham et al. 2006), as was demonstrated in a
growth chamber study using brackish marsh soils from Chesa-
peake Bay, USA, (Wolf et al. 2007). However, the ability of the
microbial community to degrade SOM is likely limited by two
factors: (i) the physical access to C compounds and (ii) the abil-
ity to produce an enzyme that can degrade relatively recalci-
trant compounds. Storage in aggregates or associated with met-
als would determine the first constraint.
The ability to produce enzymes necessary for the degra-
dation of SOM is likely dependent on the metabolic potential
of the microbial community and on microorganisms’ ability to
co-metabolize the introduced material and the SOM. In other
words, new C inputs could provide the energy necessary to pro-
duce enzymes needed to degrade a compound like suberin but
there is likely a specific subset of the microbial community able
to produce such an enzyme (Zhu et al. 2014). Little information
currently exists on specific microbial taxa capable of degrading
specific SOM components. A starting point for these types of
investigations, however, would be to consider research in con-
structed and treatment wetlands that examine organic pollu-
tant degradation. A review focused on the degradation of poly-
cyclic aromatic hydrocarbons pointed out that some constructed
wetlands can effectively remove compounds such as phenan-
threne (Haritash and Kaushik 2009). Further investigations of

these efficient constructed wetlands indicated that fungi were
likely responsible for the bulk of the degradation.
CAN MICROBIAL COMMUNITY COMPOSITION
PREDICT WETLAND FUNCTION?
Researchers have taken many different approaches towards
answering this question, including: targeting specific genes,
assessing the composition of lipids, determining community
level physiological profiles and assessing enzyme activity. One
approach has been to focus on a particular biogeochemical
transformation: methanogenesis (Kelley, Martens and Ussler
1995; Sun et al. 2012), SO4 2− reduction (Sutton-Grier et al. 2011)
or Fe (III)-reduction (Roden 2003; Keller et al. 2013). These studies
have often targeted functional genes to assess microbial compo-
sition (Table 1) simultaneous to measuring the activity. This sec-
tion will therefore begin by describing major taxonomic groups
that have been identified within wetlands, capable of specific
anaerobic metabolisms.
Methanogenesis
Methanogens are one of the best described wetland microbial
groups to date. They are phylogenetically distinct, with consid-
erable similarities between species found across different types
of wetland soils and other soil ecosystems (Bridgham et al. 2013,
reviewed therein). Studies examining methanogen composition
typically target archaeal 16S rRNA (for which methanogens com-
pose most of the wetland archaeal population) or the func-
tional gene mcrA, which codes for methyl coenzyme M reduc-
tase. Recently, a study in coastal marshes compared mcrA abun-
dance in a shotgun metagenome library to estimates using 16S
rRNA. Data from both methods agreed that methanogens com-
posed 2–10% of the bacterial/archaeal community (He et al. 2015).
Although many groups of methanogens have been described
for several years, new groups are still being identified. The
archaeal order Thermoplasmatales, which has been found in wet-
land soils (Emerson et al. 2013; Prasse, Baldwin and Yarwood
2015) and other ecosystems, was recently renamed Methanoplas-
matales when new isolates within the order were found to
produce CH4 (Paul et al. 2012). A study using stable isotope
probing (SIP) reported differences in methanogen composition
between temperate marshes dominated by Calamagrostis angus-
tifolia (reed grass) and Carex lasiocarpa (slender sedge) (Lin et al.
2015). When labeled with 13 C-acetate, Methanoscarcinaceae (ace-
toclastic methanogen) clones were more abundant in the labeled
fractions of DNA from marshes dominated by C. angustifolia,
indicating that plant species can impact the relative propor-
tion of acetoclastic versus hydrogenotrophic methanogenesis. A
studies in rice paddies, using SIP, tracked root exudates into the
methanogen community (Hori et al. 2007; Mayumi et al. 2010),
further underscoring the connection between vegetation and
methanogens.
Methanogens are typically the dominant archaeal group in
wetlands (Emerson et al. 2013; He et al. 2015; Prasse, Baldwin
and Yarwood 2015) and due to unique cell wall and mem-
brane compounds may also contribute unique molecules to
SOM. Rather than peptidoglycan layers, archaeal cell walls con-
tain S-layers composed of various proteins (Albers and Meyer
2011); ranging from simple to complex, different methanogen
groups contain different compounds. For example, Methanospir-
illum hungatei and Methanosaeta concilii have tubular paracrys-
talline sheath proteins that are resistant to degradation. Little
Yarwood 7
to nothing is known about the degradation of archaeal structural
molecules (Kögel-Knabner 2017)
Methane oxidation
One complication to examining methanogens in wetland soils
is that some methanogens carry out anaerobic CH4 oxida-
tion (AMO). This process is important in marine sediments
where methanogens oxidize CH4 through syntrophic relation-
ships with SO4 2− -reducers (Caldwell et al. 2008). Hu et al. (2014)
first reported NO3 − -dependent AMO in three freshwater wet-
lands across China representing a rural natural site, an urban
natural site and a paddy soil, and others have also observed
this phenomena (Chen, Zhou and Gu 2015; Shen et al. 2015). In
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addition to NO3 − reduction, Segarra et al. (2015) found evidence
for AMO linked to SO4 2− reduction in freshwater wetlands from
Florida, North Carolina, and Maine, USA, and Valenzuela et al.
2017 reported AMO linked to SOM reduction in tropical marsh
soil. It is not clear how widespread this process is across differ-
ent wetland types, but sequences matching AMO methanogens
have also been found in sequencing libraries in tidal freshwater
wetlands suggesting that they may be common (He et al. 2015;
Prasse, Baldwin and Yarwood 2015).
Methanotrophs were some of first organisms targeted via
13
C-SIP (McDonald et al. 2008; Dumont et al. 2011) but in most
cases those studies targeted aerobic methanotrophs using the
gene pmoA (coding for particulate CH4 monooxygenase) or bac-
terial 16S rRNA (Lüke et al. 2014). Aerobic methanotrophs belong
to 18 genera of gamma-proteobacteria (Type 2) and 5 genera of
alpha-proteobacteria (Type 1) (reviewed by Knief (2015)). Addition-
ally, aerobic methanotrophs have been identified within the
Verrucomicrobia. Methylobacter (Type 1) and Methylocystis (Type
2) have been commonly reported as most abundant OTUs in
freshwater wetlands (Knief 2015; Yun et al. 2015; Deng, Cui
and Dumont 2016), along with uncultured representatives of
Methylocystaceae 11, RA21, and RPC1 3like8, JRC3 (Knief 2015).
Targeting pmoA or bacterial specific 16S rRNA yields informa-
tion on the bacterial aerobic methanotrophs, but not the AMO
archaea, meaning the relative contribution of anaerobic to aer-
obic methanogenesis within wetlands is currently based on a
handful of studies (Deutzmann et al. 2014; Segarra et al. 2015).
AMO may be significant in freshwater wetlands, decreasing CH4
emission by over half (Segarra et al. 2015). Considerable work
remains, however, to identify which methanogens are capable
of AMO, their synergistic partners and their function under dif-
fering conditions.
Sulfate reduction
Aside from CH4 -oxidation, which can limit CH4 fluxes through
consumption, SO4 2− reduction is a competing process that can
also keep CH4 flux low (Poffenbarger, Needelman and Megoni-
gal 2011). Sulfate reducers are capable of using formate, lactate
and H2 (Plugge et al. 2011), thus competing with methanogens
for substrates. In coastal sediments, distinct depth distribu-
tions have been observed, where SO4 2− -reducers are abun-
dant in the first few centimeters but as SO4 2− is depleted
methanogens become more abundant at greater depths (Wilms
et al. 2007). In vegetated salt marshes, clear depth structures
were not observed, likely due to the heterogeneity caused by
plant rhizospheres (Castro et al. 2005). Comparing both vege-
tated and unvegetated sites, SO4 2− reduction rates were greater
in salt marshes compared to saltpans in California, USA, point-
ing to the importance of plant C to drive the process (Jackson,
Whitcraft and Dillon 2014). Sulfate reducers are often studied
 8 FEMS Microbiology Ecology 2018, Vol. 94, No. 11

Table 1. Summary of research articles using sequencing to determine microbial composition and reporting dominant wetland microbes for
general communities or targeted functional groups.

Taxonomic
groups Analysis method/gene target Wetland type Dominant organisms Reference

Fungi MiSeq/LSU Ascomycota and Forested fen Chaetothyriales Asemaninejad, Thorn

Basidomycota specific primers and Lindo 2017
Ericoid mycorrhizae
Cantharellales, graminoids and/or
ericaceous shrubs and
ectomycorrhizal root associates
Bacteria HiSeq/shotgun metagenomics Coastal estuary Bacteroides Baker et al. 2015
Planctomycetes
Chloroflexi

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Gemmatiomonas
HiSeq/16S rRNA Constructed Proteobacteria Ligi et al. 2014
wetlands (15-years
old)
Acidobacteria
Actinobacteria
Bacteriodetes
Verrucomicrobia
454/16S rRNA Natural and Proteobacteria Peralta, Ahn and
restored wetlands Gillevet 2013
Acidobacteria
Cloning and sequencing/16S rRNA Natural and Acidobacteria Hartman et al. 2008
restored wetlands
Proteobacteria
Actinobacteria
Flavobacteria-Bacteroides
Bacteria and MiSeq/16S rRNA Freshwater tidal Chloroflexi Prasse, Baldwin and
archaea wetlands Yarwood 2015
Acidobacteria
Proteobacteria
Euryarchaeota
HiSeq/16S rRNA Coastal estuary Proteobacteria He et al. 2015
(restored peat)
Chloroflexi
Bacteroides
Euryarchaeota
Functional group Analysis method/gene target Wetland Type Dominant Organisms Reference
Cellobiose SIP/MiSeq/16S rRNA Fens Firmicutes Juottonen et al. 2017
degradation
Proteobacteria
Telmatobacter-related
Acidobacteria
Verrucomicrobia
Fermenters Cloning and sequencing/16S rRNA Fens/bogs Acidobacteria Hunger, Gößner and
Drake 2015
Chloroflexi
Proteobacteria
Verrucomicrobia
Iron reducers Cloning and sequencing/16S rRNA Freshwater Geobacter sp. Lentini, Wankel and
depressional Hansel 2012
wetland
Desulfovibrio sp.
Fermenting organisms
Cloning and sequencing/16S rRNA Rice paddy Geobacter sp. Hori et al. 2010
Anaeromyxobacter
HiSeq/shotgun metagenomics Arctic peat Geobacter sp. Lipson et al. 2013
Shewanella
Acidobacteria sp.
Sulfate reducers Cloning and sequencing/dsrA Tidal freshwater Desulfarculales Kearns et al. 2016
wetlands
Desulfovibrionales
Syntrophobacterales
Firmicutes
Archaeoglobus veneficus
454 sequencing/dsrA Coastal salt Desulfobacteraceae Cui et al. 2017
marshes
Desulfobulbaceae
 Yarwood 9

Table 1. Continued

Taxonomic
groups Analysis method/gene target Wetland type Dominant organisms Reference

Methanogens Cloning and sequencing/mcrA Fens/bogs Methanoregulaceae Hunger, Gößner and

Drake 2015
Methanosarcinaceae
Methanosaetaceae
T-RFLP & cloning/16S rRNA Boreal mire Methanosarcinaceae Juottonen et al. 2008
Rice cluster II
Methanomicrobiales-associated Fen
cluster
HiSeq/shotgun metagenomics Coastal estuary Methanomicrobiales He et al. 2015
(restored peat)

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Methanobacteriales
Methanosarcinales
Methanotrophs 454 sequencing/cloning pmoA Freshwater marsh Methylobacter Yun et al. 2015
Methylocystis
13C-SIP/Cloning and sequencing/16S Bogs/fens Methylocystis Deng, Cui and Dumont
rRNA 2016
Methylobacter

by targeting the dsrA gene that codes for dissimilatory SO4 2− Fermentation
reduction (Pereyra et al. 2010). In salt marshes, dominant SO4 2− -
Many anaerobic respiring microorganisms preferentially or
reducers include delta-proteobacteria belonging to Desulfobacter-
solely use fermentation products as electron donors, but few
aceae and Desulfobulbaceae (Jackson, Whitcraft and Dillon 2014;
wetland studies include characterizing fermentation (Hunger,
Cui et al. 2017). Although studied primarily in salt or brackish
Gößner and Drake 2015). Primers have been developed and
marshes, recent evidence points to the importance of SO4 2−
applied to a bioreactor system to quantify the gene copy num-
reduction even in freshwater wetlands and peatlands, where rel-
bers of Fe-hydrogenases. Targeting the hydA gene works for
atively small populations of SO4 2− -reducing bacteria still repre-
nearly all bacteria because during fermentation reduced elec-
sent an important fate for C (Pester 2012; Hausmann et al. 2016;
tron carriers are channeled to H2 by the hydrogenase I enzyme
Kearns et al. 2016). Sulfate reducers are also capable of reduc-
(Pereyra et al. 2010), although it should be noted that these
ing Fe (III) and other metals, although there is conflicting evi-
primers are only based on sequences belonging to the Clostridi-
dence that SO4 2− -reducing bacteria can grow using these alter-
aceae. These primers have also not been used in wetland soils.
native sources (Lloyd 2003; Weber, Achenbach and Coates 2006;
Several studies have identified members of Clostridiaceae as key
Bao et al. 2018).
to fermentation (Uz and Ogram 2006; Drake, Horn and Wüst
2009), although many microbial groups include fermenters. An
Metal reduction experiment examining primary fermenters in both fens and
bogs identified numerous taxa, including members of the Aci-
As was discussed earlier, Mn (IV)- and Fe (III)-reducers have been
dobacteriaceae, Clostridiaceae, Planctomycetaceae and Veillonellaceae
observed in mineral wetlands, and Fe (III)-reduction appears to
(Hunger, Gößner and Drake 2015). Similar taxa were identified
be a major sink for C in mineral tidal and riverine wetlands
in boreal bog soils after the addition of 13 C labelled cellobiose
(Neubauer et al. 2005; Sutton-Grier and Megonigal 2011). Many
(Juottonen et al. 2017). In particular, members of the Clostridiaceae
bacterial isolates capable of Fe (III) reduction can also reduce
and Veillonellaceae (both within phylum Firmicutes) composed
Mn (IV) and trace metals (Poole 2004). Trace metals including
as much as 69% of the labelled fraction of DNA, underscoring
lead, zinc and copper have been shown to accumulate in the Fe
their role as important fermenters (Juottonen et al. 2017). Prod-
(III) plaques surrounding wetland plant roots (Xu et al. 2018). In
ucts from primary fermentation (i.e. organic acids and alcohols)
addition to frequently studied Fe(III)-reducers, such as Geobac-
are often not associated with particular fermenting groups, but
ter spp. (members of the deta-proteobacteria) and Shewanella spp.
Juottonen et al. (2017) observed a positive relationship between
(members of the gamma-proteobacteria), Fe(III)-reduction has also
Veillonellaceae abundance and propionate concentration. There
been observed in other classes of Proteobacteria, and in the phyla
are likely numerous microbial groups capable of fermentation,
Firmicutes, Crenarchaeota, Euryarchaeota and Acidobacteria (Weber,
as was demonstrated by shotgun sequencing of an anaerobic
Achenbach and Coates 2006). Unlike methanogenesis or SO4 2−
aquifer (Wrighton et al. 2012). That study included the discov-
reduction, the variety of physiological strategies used by Fe (III)-
ery of many uncultured fermenters belonging to candidate phyla
reducers excludes using a single or a handful of functional gene
OD1, OP11 and others, again highlighting the potential difficulty
markers to examine composition. A metagenomic study in arc-
in connecting phylogenetic structure to function.
tic peat described Fe (III)-reducing communities by examining
genes that coded for decaheme cytochromes (Lipson et al. 2013),
and this approach holds promise for more thoroughly examin-
16S rRNA: general bacterial and archaeal communities
ing metal-reducing populations. Currently, there are no publica-
tions that directly examine Fe(III)-reducer diversity paired with In addition to studies that have measured functional genes
function, but this is understandable given the diversity of organ- and the activities of specific metabolic groups, studies have
isms that may be involved. targeted the 16S rRNA or in a few studies used shotgun
 10 FEMS Microbiology Ecology 2018, Vol. 94, No. 11
metagenomics (Table 1). The advantage of using 16S rRNA
or shotgun metagenomics is the ability to simultaneously
observe shifts in many functional groups. The major dis-
advantage is that microbial plasticity and functional redun-
dancy hamper efforts to connect phylogenetic groups to func-
tion. Metabolic plasticity refers to the adaptation of a sin-
gle organism to differences in environmental conditions. An
example might be a change in C use efficiency, an important
metric given that microbial-derived molecules may be prefer-
entially stored as SOM. Although microbial community level
physiological profiles is dependent on the composition of
microbes and on their individual responses to current condi-
tions (Roller and Schmidt 2015), measurements of community
level physiological profiles are taken in bulk (Geyer et al. 2016)
and therefore little knowledge exists about how microbial com-
position impacts community level physiological profiles.
In wetlands, metabolic plasticity refers to the ability of a
single cell belonging to a taxonomic group as specific as a
species or a strain to belong to multiple functional guilds. A
study that directly quantified microbial plasticity and func-
tional redundancy in freshwater bacterioplankton reported that
metabolic plasticity was an inherent trait of the microbial
community. In other words, the community displayed metabolic
plasticity regardless of environmental conditions and the
metabolic capacity of the community was bounded by the taxo-
nomic groups present (Comte et al. 2013).
16S rRNA surveys are typically unable to provide fine taxa-
nomic resolution due to the conserved nature of the molecule
and high throughput sequencing strategies that typically only
target 200–500 bp. Studies that have examined wetland micro-
bial communities via 16S rRNA amplification often report the
relative abundances of dominant phyla and classes of Proteobac-
teria (Table 1), with only limited mentions of specific sequence
matches to a select few organisms. For example, Acidobacteria
and Proteobacteria have been reported as dominant phyla in nat-
ural, restored and created wetlands (Hartman et al. 2008; Per-
alta, Ahn and Gillevet 2013; Prasse, Baldwin and Yarwood 2015).
Phyla level classification are not helpful in linking composi-
tion to function, however, as most phyla contain members of
multiple functional guilds (Table 2). Reporting the abundance
of different genera would better align to function, but this is
difficult within a scientific publication given the large num-
bers of taxonomic groups within each study and the necessity
to somehow simplify data in order to look for trends. Consistent
sequence analysis standards, data provided in spreadsheet form
and its availability to the research community would improve
our ability to compare wetland studies. There has not been a
published meta-analysis of 16S rRNA sequences across multiple
wetland types, but the quickly expanding field of wetland micro-
biology combined with next generation sequencing means that
data likely exist to carry out such an analysis (Neori and Agami
2017).
This kind of 16S rRNA meta-analysis would be interesting
and could yield new insights about the similarity and differ-
ences between microorganism in different wetland types and
factors that drive distribution. However, links to function would
still be difficult. In spite of efforts to create programs such as
PICRUSt (Langille et al. 2013) and Tax4fun (Aßhauer et al. 2015)
that predict function based on 16S rRNA and shotgun metage-
nomic analysis, the information on specific wetland taxa is still
sparse. There is still a lot of research needed to describe indi-
viduals within the microbial community and understand their
functional capacities.
Functional redundancy further complicates the connections
between composition and function. For example, virtually all
denitrifying bacteria can also carry out aerobic respiration
(Jones et al. 2008) and as mentioned before many microbial
species can reduce multiple metals. In Comte et al. (2013)
functional redundancy, within the bacterioplankton commu-
nity, varied under different environmental conditions. For exam-
ple, the ability to access C substrate depended both on the
redox conditions and the capacity of individuals belonging
to the community. The number of taxa found in 16S rRNA
or shotgun metagenomic studies would suggest that func-
tional redundancy is high in wetland microbial communities.
Although we know that these communities are diverse, DNA-
based methods may artificially inflate estimates of functional
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redundancy. The DNA-based approach cannot distinguish
between active and dormant cells (Lennon and Jones 2011) nor
distinguish relic DNA (Dlott et al. 2015; Carini et al. 2016). Also
contributing to issues related to functional redundancy, most
studies characterize the community at a single time point. Most
functional data are gathered over repeated measures, however,
resulting in structure and function mismatches.
Returning to the question that began this section, there
currently seems to be more studies that report mismatches
between composition and function rather than those that
observe strong connections. However, this by no means, implies
that assessing microbial composition is fruitless. Rather the cur-
rent state of knowledge concerning wetland microorganisms is
such that there is a virtually inexhaustible list of queries relat-
ing to the role of microorganisms in wetland functions such
as SOM formation, but the science is quickly expanding to
address this challenge and evidence for more direct linkages
between composition and function are likely in the near future.
The last section of the review will describe some of the newest
research and make suggestions for future endeavors that move
us closer to this future reality.
THE CURRENT STATUS AND FUTURE OF
WETLAND MICROBIAL SOM RESEARCH
Key knowledge gaps in wetland microbial communities as it
relates to plant litter decomposition and SOM formation include:
(i) What factors control microbial access to and decomposition
of plant litter and SOM? (ii) How does microbial community
structure shape C fate, across different wetland types? (iii) What
types of plant and microbial molecules contribute to SOM accu-
mulation? Resolving these unknowns requires studies that span
many different wetland types and account for temporal changes
at multiple scales. They also require integrating microbiological
and biogeochemical approaches.
A synthesis of SOM theory identified eight mechanisms lead-
ing to SOM formation (Schmidt et al. 2011). These mechanisms
are: inherent recalcitrance of molecules, condensation reac-
tions, fire residues (e.g. charcoal), rhizosphere inputs, physical
protection due to aggregation, organo-mineral complexes, deep
soil C, freezing/thawing and microbial products. Several of these
mechanisms have already been touched on within this review
but considering this list and the variety of wetland types, most
if not all of these mechanisms are likely at work within wetland
soils. Methods such as 13 C labelling can be used to track C into
the active fraction of the community (McDonald et al. 2008; Deng,
Cui and Dumont 2016; Juottonen et al. 2017); different labelled

Table 2. Major bacterial phyla and classes identified in wetland studies and known metabolic capability within each group.
Aerobic Mn (IV)
Taxa respiration1 Fermentation Denitrification2 reduction
Proteobacteria
α X X X
β X X X
δ X X X
γ X X X
Firmicutes X X X X
X X X X
Acidobacteria
X X
Euryarchaeota
X X
Crenarchaeota
1
Chen and Strous 2013.
2
Jones et al. 2008.
3
Weber, Achenbach and Coates 2006.
4
Thauer, Stackebrandt and Hamilton 2007.
5
Fe (II) oxidation.
6
NH3 oxidation & Fe (II) oxidation.
7
Fe (II) oxidation.
8
Fe (II) oxidation.
9
NH3 oxidation.
substrates stimulates different members of the microbial com-
munity (Braeckevelt et al. 2007). For example, pulse labeling wet-
land plants with 13 C-CO2 allows root exudates to be tracked into
the microbial community. These experiments can help iden-
tify the decomposing community and measure priming of SOM
under different conditions (Angst et al. 2017). Pulse labeling has
been carried out in rice paddies (Qiu, Conrad and Lu 2009), but
could be expanded to mixed plant communities and combined
with methods that examine C incorporation into aggregates and
binding on metal surfaces.
Another strategy for understanding microbial decomposition
is to assess the functional capacity of the community using com-
munity level physiological profiles or enzyme assays. Commu-
nity level physiological profiles have been used to character-
ize constructed wetlands (Zhang et al. 2010; Weber and Legge
2011), identifying differences between planted and unplanted
systems. They were also used in combination with leaf lit-
ter bags to assess decomposition in freshwater streams (Sam-
paio et al. 2008); community level physiological profiles differed
between riverine and depressional wetlands in that study. Cur-
rent knowledge of enzymes was reviewed recently (Burns et al.
2013), and methodological considerations associated with wet-
land soils is discussed by Dunn et al. (2014). Assays to assess phe-
nol oxidase and test the enzymatic latch hypothesis have been
conducted in both temperate (Pinsonneault, Moore and Roulet
2016) and mangrove peatlands (Saraswati et al. 2016). In both
cases, results of these enzyme assays supported the role of the
enzymatic-latch in C accumulation.
Physical characterization of wetland soils can also shed light
on mechanisms for C storage. For example, Xiao et al. (2014) frac-
tioned estuary soils into aggregate size classes and found that
polycyclic aromatic hydrocarbons were preferentially stored
within water stable aggregates. Aggregate fractions can also be
assessed for microbial communities as was done in agricul-
tural soils, where researchers reported differences in commu-
nity composition between different size classes (Kim and Crow-
ley 2013). In their review, Han et al. (2016) discussed that different
size fractions are also associated with different C molecules, for
example microbial-derived molecules are often more abundant
Yarwood 11
Fe (III) SO4 −2 CH4 Other
reduction3 reduction4 Methanogenesisoxidation metabolism
X X5
X6
X X
X X X7
X X X
X8
X X X X
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X X9
in micro-aggregates. As mentioned early and unique to wet-
lands, characterization of metal concretions and nodules may
also offer new insights into SOM storage mechanisms (Hickey,
McDaniel and Strawn 2008).
The fate of wetland C is dependent on the microbial com-
munity and the environment that it experiences, both of which
define the interactions between different taxa and functional
guilds. Syntrophy can be broadly defined as one organism living
off the products of another organism (Morris et al. 2013). These
interactions are important in many microbial ecosystems and
central to understanding the anaerobic processes within wet-
lands where energy yields are relatively low and where prod-
ucts are not diffusion limited, at least during part of each year.
Although we know that these relationships exist in wetlands,
the extent of these relationships and the identity of its mem-
bers is largely unknown. Culturing does not easily isolate organ-
isms that live on the ‘energetic edge’ and a recent study exam-
ining syntrophy in fens and bogs through DNA analysis reported
that 40% of family level classifications had no match to current
databases (Hunger, Gößner and Drake 2015).
Syntrophobacter spp. have been found in many types of
wetlands (Lueders, Pommerenke and Friedrich 2004; Hunger,
Gößner and Drake 2015) and are likely one of the most com-
mon groups of syntrophic bacteria. The first-described Syntro-
phobacter spp. are able to reduce S when available in the soil
matrix, but when oxidized S is depleted they oxidize propionate
to acetate and reduce H+ to H2 (Boone and Bryant 1980). The
resulting acetate and H2 can support methanogens or aceto-
gens. Initially Syntrophobacter spp. were speculated to be obli-
gate mutualists, dependent on methanogens/acetogens to keep
H2 concentrations low so that enough energy could be gained.
A few years later, however, Syntrophobacter spp. were grown in
pure culture, demonstrating that at least some members are fac-
ultative mutualists (Wallrabenstein 1994). Additional described
Syntrophobacter spp. can only degrade butyrate or propionate
in the presence of their methanogen partner and must be co-
cultured (Stams and Plugge 2009). Another commonly studied
facultative syntrophic species is Ruminococcus albus. This species
 12 FEMS Microbiology Ecology 2018, Vol. 94, No. 11
can ferment sugars independent of a syntrophic partner, but
can gain more energy when H2 -consuming methanogens are
present (Stams and Plugge 2009). R. albus is common in the
rumen system, but has not been detected in wetlands (Stams
and Plugge 2009), although it is likely that functionally similar
organisms are present.
Targeting mRNA may be one way that microbial structure
and function can be better linked, as Juottonen et al. (2008)
demonstrated by measuring mcrA and CH4 flux. The advan-
tage of methanogens over other functional groups, however, is
their relatively low diversity. Furthermore, it may be difficult to
observe shifts in mRNA when conditions are relatively stable or
when genes are constitutively expressed (Moran et al. 2013). For
example, in continuously saturated wetlands, mRNA may not be
particularly helpful because the enzymes that mediate anaero-
bic metabolism have already been translated. Metaproteomics
offers another approach that could help to better link struc-
ture and function. In a treatment wetland, metaproteomics was
used to identify rhizosphere microorganisms capable of degrad-
ing toluene (Lünsmann et al. 2016).
The challenge faced in wetland C cycling is not conceptualiz-
ing the multiple interactions that could take place, especially in
the rhizosphere, but designing experiments and adopting meth-
ods that can detect them. One approach is to characterize micro-
bial communities in space and time (using DNA sequencing,
mRNA sequencing or other biomarkers) and construct pairwise
correlation matrices between the relative abundances of micro-
bial taxa or functional groups (Boon et al. 2014). Significant pos-
itive correlations might help to target subsets of the commu-
nity that are mutualists, but they also may only be evidence of
shared preferences to environmental conditions (Faust and Raes
2012). Regardless of the method of characterization studies need
to reflect the correct scale for the question being asked and con-
tain sufficient replication as to yielded meaningful data.
Modeling SOM formation and stability also requires fine tun-
ing our understanding of the fates of individual C compounds
such as plant lignin or microbial cell walls. Pyrolysis GC–MS has
been used to characterize the molecules that compose SOM, as
was done in a survey of forest soils across a latitudinal gradient
spanning tundra to tropical soils (Vancampenhout et al. 2009).
Tundra soils contained more plant-derived molecules as might
be expected from a slower decomposition process. Applied to
coastal wetlands in South Africa, pyrolysis GC–MS analyzed sub-
soils contained SOM that was more degraded and contained
polyphenols, but surfaces soils contained more plant-derived
lignin (Carr et al. 2010). Sediment cores from a bay in Ireland con-
tained both plant and microbial-derived molecules, and proteins
with hydrophobic domains were in some of the deepest areas
sampled (Mylotte et al. 2015). Other methods for SOM charac-
terization include 13C NMR and chemical fractionation followed
by Fourier transform ion cyclotron resonance mass spectrome-
try (Tfaily et al. 2015), the later method provides high resolution
compound data and is just beginning to be used in peatlands
and other wetland soils.
CONCLUDING REMARKS
Wetlands have fascinated microbial ecologists for over a cen-
tury. They shaped the work of Sergei Winogradskyi (Ackert 2007)
and in essence led to the founding of microbial ecology. Wet-
lands have also served as model environments inspiring and
informing work as broad as microbial fuel cell technology and
waste water treatment. SOM accumulations is an important
ecosystem service of wetlands and there is currently evidence
for a variety of storage mechanisms across different wetland
types. The enzymatic latch and the accumulation of undecom-
posed plant material is likely more important in histic north-
ern peatlands compared to temperate mineral wetlands. Min-
eral wetlands likely store C via physical and chemical protection,
although the details of these processes are yet fully described.
Microbial degradation of above-ground plant litter likely begins
before the material enters the soil and the role of fungi in wet-
lands needs more investigation. The interactions between C and
metals may influence SOM storage capacity and may control
microbial degradation. Changes in wetland conditions such as
change in flooding frequency and increase CO2 may lead to loss
of C stocks, but more information on the alteration in micro-
bial communities is needed to make clear predictions. Analyti-
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cal tools for measuring the microbial community and SOM have
been developed and are increasingly applied across different
wetland systems, resulting in quickly expanding knowledge of
these complex systems. Wetland researchers are increasingly
applying multi-pronged approaches that bring together micro-
bial ecology, biogeochemistry and modeling to better under-
stand the fate of C in wetlands around the world.
ACKNOWLEDGMENTS
Thanks to Dr. Peter Bottomley and Dr. Andrew Baldwin for
reviewing early drafts of this review and for the comments of
four anonymous reviewers.
Conflicts of interest. None declared.
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