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NEWS AND VIEWS
PERSPECTIVE
Do bacterial and fungal communitiesassemble differently during primarysuccession?
S . K. SCHMIDT,* D. R. NEMERGUT,†‡
J . L . DARCY* and R. LYNCH**Department of Ecology and Evolutionary Biology, University of
Colorado, Boulder, CO, 80309, USA; †Institute of Arctic andAlpine Research, University of Colorado, Boulder, CO 80309,
USA; ‡Environmental Studies Program, University of Colorado,
Boulder, CO 80309, USA
High-throughput sequencing technologies are now allow-
ing us to study patterns of community assembly for
diverse microbial assemblages across environmental gra-
dients and during succession. Here we discuss potential
explanations for similarities and differences in bacterial
and fungal community assembly patterns along a soil
chronosequence in the foreland of a receding glacier.
Although the data are not entirely conclusive, they do
indicate that successional trajectories for bacteria and
fungi may be quite different. Recent empirical and
theoretical studies indicate that smaller microbes (like
most bacteria) are less likely to be dispersal limited
than are larger microbes – which could result in a more
deterministic community assembly pattern for bacteria
during primary succession. Many bacteria are also better
adapted (than are fungi) to life in barren, early-succes-
sional sediments in that some can fix nitrogen and carbon
from the atmosphere – traits not possessed by any fungi.
Other differences between bacteria and fungi are
discussed, but it is apparent from this and other recent
studies of microbial succession that we are a long way
from understanding the mechanistic underpinnings of
microbial community assembly during ecosystem succes-
sion. We especially need a better understanding of global
and regional patterns of microbial dispersal and what
environmental factors control the development of micro-
bial communities in complex natural systems.
Keywords: bacteria, climate change, community ecology,
fungi, landscape genetics, phylogeography
Received 24 October 2013; revised xxxx; accepted 12 November
2013
The conceptual framework for understanding primary suc-
cession was initially developed from the study of plant
systems, with the earliest work dating to 1685 (Clements
1916), but also grew out of studies of pedogenesis (soil
development, e.g. Jenny 1980) and more recently from gen-
eralized community assembly theory (Vellend 2010; Nemer-
gut et al. 2013). Plants, microbes and soils share obvious
connections, but it was not until the rise of high-throughput
sequencing technologies that phylogenetic community pro-
files of multiple microbial communities could be rapidly
inventoried. We now have the opportunity to test ecological
hypotheses developed from the study of macroscopic plants
and animals, as well as emerging hypotheses specific to
microorganisms (Nemergut et al. 2013). Studies of microbial
succession are also becoming more important because global
warming is causing unprecedented rates of glacial retreat
especially in high-elevation and high-latitude environments
where the rate of plant colonization is quite slow compared
with that of microbes (Fig. 1).
Brown & Jumpponen (2013) studied bacterial and fungal
community succession and assembly along a chronose-
quence of soils created by the receding Lyman Glacier in
the northern Cascade Range. By comparing community
assembly of bacteria and the fungi in these new soils, they
address several specific questions, including: Do bacterial
and fungal communities follow similar assembly trajecto-
ries along the chronosequence? Does the presence of plants
alter the assembly trajectories for bacteria and fungi? The
study of Brown & Jumpponen (2013) can also be viewed in
light of the debate about whether historical or deterministic
factors are more important in controlling community
assembly during succession. This debate originated from
the deterministic view of Clements (e.g. 1916, 1936) and
the more historical view of Gleason (e.g. 1926) and has
recently been addressed in studies of microbial systems
(e.g. Peay et al. 2012; Ferrenberg et al. 2013). Here, we dis-
cuss the results of Brown & Jumpponen (2013) from the
perspective of this debate and with respect to the growing
body of knowledge about microbial dispersal, biogeogra-
phy and biogeochemistry.
Perhaps the most interesting finding of Brown & Jump-
ponen (2013) was that a greater fraction (19%) of fungal
OTUs displays nonrandom patterns of occurrence along
the chronosequence compared with bacterial OTUs (9.5%).
However, when examined as a whole, bacterial communi-
ties were more affected by both distance along the chrono-
sequence and vegetation cover than were fungal
communities. In addition, bacterial communities converged
along the chronosequence, whereas fungal community
assembly appeared to be more stochastic (less determinis-
tic) and showed no evidence of convergence towards one
community type (Brown & Jumpponen 2013).
Although the data of Brown & Jumpponen (2013) are by
no means conclusive, they do hint at different trajectories ofCorrespondence: Steve Schmidt, Fax: 303-492-8699;
E-mail: Steve.Schmidt@Colorado.edu
© 2013 John Wiley & Sons Ltd
Molecular Ecology (2014) 23, 254–258
succession for bacteria and fungi at this site. If bacterial
communities converge on one community type during suc-
cession, and fungi do not, this may indicate that bacterial
communities assemble in a more deterministic fashion than
do fungi. One likely explanation for this pattern is that
fungi may be more dispersal limited than bacteria and
therefore more prone to historical (stochastic) effects at this
site (Fig. 2). Some recent studies indicate that early-succes-
sional Betaproteobacteria (e.g. Polaromonas spp.) are not dis-
persal limited at the global scale (Darcy et al. 2011),
whereas larger microbes like algae and zoosporic fungi
(both common in periglacial environments) show more
divergent biogeographic patterns (and therefore perhaps
dispersal limitation) at global and regional scales (De
Wever et al. 2009; Schmidt et al. 2011; Naff et al. 2013).
Recent modelling studies also support a difference in dis-
persal capabilities between smaller (e.g. bacteria) and larger
(e.g. fungi) microbes. Wilkinson et al. (2012) showed that
there is a very low probability that microbes greater than
20 lm in diameter can undergo passive dispersal between
continents and that the successful dispersal of small
microbes is due to their greater abundance and their longer
residence times in the atmosphere compared with larger
microbes. Thus, both empirical and theoretical studies point
to a more consistent ‘propagule rain’ (sensu Brown & Jump-
ponen 2013) of bacteria at early-successional sites (Fig. 2).
A more consistent propagule rain for bacteria could
reduce or eliminate priority effects for bacterial communi-
ties resulting in more deterministic community assembly
across the landscape compared with fungi. Other research
Fig. 1 Repeat photography of a site in
the High Andes of Per�u where rapid gla-
cial retreat is exposing large tracts of
land that are rapidly colonized by
microbes (months to years) but only
slowly colonized by plants (decades to
centuries). The top photograph was taken
in 2005 and the bottom in 2010 (the per-
son in each photograph is standing in
approximately the same location). The
photographer was standing at about
5200 m above sea level near the ‘100-m
site’ viewable in an aerial photograph of
the site previously published in Schmidt
et al. (2009). The distance from the per-
son to the closest edge of the ice is
approximately 20 and 200 meters in the
top and bottom photos, respectively.
Note the edge of a lake that formed
between 2005 and 2010 (lower left corner
of bottom photo). Photograph credits
S.K. Schmidt and J.L. Darcy.
© 2013 John Wiley & Sons Ltd
NEWS AND VIEWS: PERSPECTIVE 255
has shown that priority effects can lead to greater diver-
gence in fungal community assembly (Peay et al. 2012) and
are more likely to occur when the rate of propagule input
is low (Chase 2003). For example, priority effects deter-
mined the ultimate fungal community structure of two
ectomycorrhizal species on pine roots (Kennedy & Bruns
2005). Likewise, complex wood decomposing fungal
communities can be driven to significantly different succes-
sional outcomes by the order of addition of community
members (Fukami et al. 2010).
Another potential reason that bacteria and fungi have
different early-successional trajectories is that bacteria exhi-
bit a broader range of physiologies than do fungi and thus
are more likely to be successful colonists of the oligo-
trophic, plant-free soils near the glacier terminus. Early-
successional bacteria can be photoautotrophs, heterotrophs
or chemoautotrophs and many can fix atmospheric nitro-
gen (Nemergut et al. 2007; Schmidt et al. 2008b; Duc et al.
2009), whereas fungi are all heterotrophs and none can fix
nitrogen. Thus, fungi are more dependent than bacteria on
fixed sources of carbon and nitrogen and may not have as
many available niches before there is significant organic
matter build-up during succession. Indeed, it may be that
many of the fungi present in recently deglaciated sites are
actually dormant (due to lack of organic matter) as origi-
nally suggested by Jumpponen (2003), in which case their
distribution across the landscape would probably be more
stochastic due to the dispersal constraints discussed above.
Alternatively, wind-blown particles tend to accumulate in
protected pockets, for example next to rocks (Swan 1992),
which would cause a very nonuniform (seemingly stochas-
tic) accumulation of organic matter (and therefore fungi)
across the early-successional landscape. Brown & Jumppo-
nen (2013) also point out that many of the fungal OTUs at
their sites are related to fungi known to be associated with
insects. This observation supports the hypothesis of
Hodkinson et al. (2002) and Swan (1992) that wind-blown
arthropods can be important sources of organic matter in
recently deglaciated environments.
As highlighted by Brown & Jumpponen (2013) and other
authors, one of the big mysteries surrounding the early
stages of microbial succession is determining the source of
carbon and energy for the early colonists. In addition to
allochthonous (mostly wind-blown) carbon (C) inputs
discussed above, the two other major sources of C to
early-successional soils are ancient C (Welker et al. 2002;
Bardgett et al. 2007; Sattin et al. 2009) and C fixed autoch-
thonously by photo- and chemoautotrophs (Nemergut et al.
2007; Schmidt et al. 2008b). The relative contribution of
each of these C sources to the overall pool of C in early-
successional soils probably has a major effect on the struc-
ture of the resulting microbial communities (Fierer et al.
2010). For example, sites with relatively high levels of
ancient C, or high inputs of wind-blown C, might be
dominated by heterotrophs early in succession. By contrast,
sites with low levels of wind-blown and ancient C would
probably be dominated by autotrophs early in microbial
succession. As sunlight is abundant at the soil surface
before plants colonize periglacial soils, it is logical to
assume that photoautotrophs will be important players in
most newly deglaciated soils especially in areas with low
levels of soil carbon. However, other factors may stunt the
development of microbes early in succession, such as limi-
tations of essential nutrients (Yoshitake et al. 2007; G€orans-
son et al. 2011; Schmidt et al. 2012). Given the importance
of C and other elements for the development of microbial
communities, more information is needed on the geochem-
istry and aeolian inputs of nutrients to all of the early-
successional sites presently being studied by microbial
ecologists (Mladenov et al. 2012).
Finally, the relationship between plant and soil micro-
bial communities in early-successional sites should be
highly correlated (Blaalid et al. 2012; Knelman et al. 2012)
as the nutrient cycling cascades catalysed by microorgan-
isms in plant-free soils are likely to strongly influence the
success of plant colonization and because plants add sub-
stantial inputs of carbon to the soils through both litter
and root exudates. Most importantly, plants form symbi-
otic relationships with many soil bacteria and fungi and
should therefore skew microbial community assembly
towards symbiotic heterotrophs. Therefore, it was some-
what surprising that Brown & Jumpponen (2013) found
that the presence of plants played a very minor role in
the distribution of fungal OTUs relative to bacterial OTUs
at the community level. This difference could be
explained by dispersal limitations of fungi relative to bac-
teria as discussed above. Previous studies have shown
that inoculum levels for the most common type of plant
Propagules
Time
Fig. 2 The influence of the timing and contents of ‘propagule rain’ is depicted. In some cases, dispersal and establishment are successful (solid blue arrows). In other cases, dispersal is not successful and the microorganisms perish in transit or on arrival (dashed lines) or may be poorly adapted to the new environment (teal hexagons). Priority effects may also play an important role in microbial community assembly during suc-cession. For example, the red ovals and yellow squares arrive first, gaining a competitive advantage as they monopolize resources. Later migrants (small green circles) may not be com-
petitive due to their lower relative abundance and the seques-tration of limiting nutrients by earlier colonists (e.g. the red ovals). Had the green circles arrived first instead of the red ovals, they may have been more successful and the community would have assembled differently. See last page for larger image.
© 2013 John Wiley & Sons Ltd
256 NEWS AND VIEWS: PERSPECTIVE
symbionts, arbuscular mycorrhizal fungi, are often below
detection limits in early-successional soils – favouring
weedy, nonmycorrhizal plants early in succession (Miller
1979; Schmidt et al. 2008a). However, it is notable that,
when examined at the community level, the presence of
specific plant taxa had a significant influence on fungal,
as well as bacterial composition (Brown & Jumpponen
2013).
It would be interesting to re-examine the data of Brown
& Jumpponen (2013) using a nested, multivariate approach
to partition the relative influence of distance along the
chronosequence vs. plant cover (presence or absence of
vegetation as well as plant species type) on bacterial and
fungal community composition as well as the relationships
between these two groups. Likewise, a deeper exploration
of soil physiochemical parameters and/or the use of null
deviation analyses could help identify the cause of the dif-
ference in patterns of bacterial distribution along the chro-
nosequence. Brown & Jumpponen (2013) posit that
bacterial assembly processes are more stochastic very early
in succession, but not later in succession, a pattern that has
been documented in other systems (e.g. Ferrenberg et al.
2013). However, it is also possible that these seemingly
stochastic patterns are actually due to heterogeneity in
environmental filters (e.g. soil organic matter as discussed
above) and that plant invasion serves to homogenize the
landscape, making assembly appear to be more determinis-
tic in older soils.
Overall, the study of Brown & Jumpponen (2013) and
other recent studies (e.g. Zumsteg et al. 2012) illuminate
the importance of studying more than just one component
of the microbial community and point the way to future
work needed to understand the patterns they report. Espe-
cially needed are studies of the relative dispersal abilities
of microbial groups and studies of nutrient levels, inputs
and limitations in early-successional systems. New, high-
throughput sequencing technologies have allowed us to
finally describe the spatial and temporal patterns of micro-
bial communities, but mechanistic studies that isolate the
relative importance of the individual drivers of microbial
community assembly lag far behind.
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© 2013 John Wiley & Sons Ltd
258 NEWS AND VIEWS : PERSPECT IVE
Fig. 2 The influence of the timing and contents of ‘propagule rain’ is depicted. In some cases, dispersal and establishment are successful (solid blue arrows). In other cases, dispersal is not successful and the microorganisms perish in transit or on arrival (dashed lines) or may be poorly adapted to the new environment (teal hexagons). Priority effects may also play an important role in microbial community assembly during succession. For example, the red ovals and yellow squares arrive first, gaining a competitive advantage as they monopolize resources. Later migrants (small green circles) may not be competitive due to their lower relative abundance and the sequestration of limiting nutrients by earlier colonists (e.g. the red ovals). Had the green circles arrived first instead of the red ovals, they may have been more successful and the community would have assembled differently.
Propagules
Time
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