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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 (2014) 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 (2014) 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 (2014) 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 (2014) 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 2014).

Although the data of Brown & Jumpponen (2014) 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 2014) 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 (2014) 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 (2014) 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 (2014) 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.

© 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

2014).

It would be interesting to re-examine the data of Brown

& Jumpponen (2014) 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 (2014) 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 (2014) 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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