Molecular Ecology (2014) 23, 254–258
NEWS AND VIEWS
PERSPECTIVE
Do bacterial and fungal communities assemble differently during primary succession? S. K. SCHMIDT,* D. R. NEMERGUT,†‡ J . L . D A R C Y * and R . L Y N C H * *Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA; †Institute of Arctic and Alpine Research, University of Colorado, Boulder, CO 80309, USA; ‡Environmental Studies Program, University of Colorado, Boulder, CO 80309, USA
High-throughput sequencing technologies are now allowing us to study patterns of community assembly for diverse microbial assemblages across environmental gradients 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-successional 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 succession. We especially need a better understanding of global and regional patterns of microbial dispersal and what environmental factors control the development of microbial communities in complex natural systems. Keywords: bacteria, climate change, community ecology, fungi, landscape genetics, phylogeography Received 24 October 2013; revised 2013
xxxx; accepted 12 November
The conceptual framework for understanding primary succession was initially developed from the study of plant Correspondence: Steve Schmidt, Fax: 303-492-8699; E-mail: [email protected]
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 generalized community assembly theory (Vellend 2010; Nemergut 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 profiles 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 chronosequence 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 trajectories 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 discuss the results of Brown & Jumpponen (2014) from the perspective of this debate and with respect to the growing body of knowledge about microbial dispersal, biogeography and biogeochemistry. Perhaps the most interesting finding of Brown & Jumpponen (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 communities were more affected by both distance along the chronosequence 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 deterministic) 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 of
© 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 255 Fig. 1 Repeat photography of a site in the High Andes of Per u where rapid glacial 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 person 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 person 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.
succession for bacteria and fungi at this site. If bacterial communities converge on one community type during succession, 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-successional Betaproteobacteria (e.g. Polaromonas spp.) are not dispersal 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). © 2013 John Wiley & Sons Ltd
Recent modelling studies also support a difference in dispersal 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 & Jumpponen 2014) of bacteria at early-successional sites (Fig. 2). A more consistent propagule rain for bacteria could reduce or eliminate priority effects for bacterial communities resulting in more deterministic community assembly across the landscape compared with fungi. Other research
256 N E W S A N D V I E W S : P E R S P E C T I V E
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 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.
has shown that priority effects can lead to greater divergence 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 determined 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 successional 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 exhibit a broader range of physiologies than do fungi and thus are more likely to be successful colonists of the oligotrophic, plant-free soils near the glacier terminus. Earlysuccessional bacteria can be photoautotrophs, heterotrophs or chemoautotrophs and many can fix atmospheric nitrogen (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 originally 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 stochastic) accumulation of organic matter (and therefore fungi) across the early-successional landscape. Brown & Jumpponen (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 autochthonously 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 earlysuccessional soils probably has a major effect on the structure 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 limitations of essential nutrients (Yoshitake et al. 2007; G€ oransson 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 geochemistry and aeolian inputs of nutrients to all of the earlysuccessional sites presently being studied by microbial ecologists (Mladenov et al. 2012). Finally, the relationship between plant and soil microbial communities in early-successional sites should be highly correlated (Blaalid et al. 2012; Knelman et al. 2012) as the nutrient cycling cascades catalysed by microorganisms in plant-free soils are likely to strongly influence the success of plant colonization and because plants add substantial inputs of carbon to the soils through both litter and root exudates. Most importantly, plants form symbiotic relationships with many soil bacteria and fungi and should therefore skew microbial community assembly towards symbiotic heterotrophs. Therefore, it was somewhat 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 bacteria as discussed above. Previous studies have shown that inoculum levels for the most common type of plant
© 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 257 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 difference in patterns of bacterial distribution along the chronosequence. 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 deterministic 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. Especially needed are studies of the relative dispersal abilities of microbial groups and studies of nutrient levels, inputs and limitations in early-successional systems. New, highthroughput sequencing technologies have allowed us to finally describe the spatial and temporal patterns of microbial communities, but mechanistic studies that isolate the relative importance of the individual drivers of microbial community assembly lag far behind.
References Bardgett RD, Richter A, Bol R et al. (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biology Letters, 3, 487–490. Blaalid R, Carlsen T, Kumar S et al. (2012) Changes in root-associated fungal communities along a primary succession gradient analyzed by 454 pyrosequencing. Molecular Ecology, 21, 1897– 1908. Brown SP, Jumpponen A (2014) Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Molecular Ecology, 23, 481–497. Chase JM (2003) Community assembly: when should history matter? Oecologia, 136, 489–498. Clements FE (1916) Plant Succession: An Analysis of the Development of Vegetation (No. 242). Carnegie Institution of Washington, Washington, DC.
© 2013 John Wiley & Sons Ltd
Clements FE (1936) Nature and structure of the climax. Journal of Ecology, 24, 252–284. Darcy JL, Lynch RC, King AJ, Robeson MS, Schmidt SK (2011) Global distribution of Polaromonas phylotypes - evidence for a highly successful dispersal capacity. PLoS ONE, 6, e23742. doi:10.1371/ journal.pone.0023742. De Wever A, Leliaert F, Verleyen E et al. (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proceedings. Biological sciences/The Royal Society, 276, 3591–3599. Duc L, Noll M, Meier BE, B€ urgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding Alpine glacier. Microbial Ecology, 57, 179–190. Ferrenberg S, O’Neill SP, Knelman JE et al. (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. The ISME Journal, 7, 1102–1111. Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Research in Microbiology, 161, 635–642. Fukami T, Dickie IA, Wilkie JP et al. (2010) Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecology Letters, 13, 675–684. Gleason HA (1926) The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club, 53, 7–26. G€ oransson H, Venterink HO, B a ath E (2011) Soil bacterial growth and nutrient limitation along a chronosequence from a glacier forefield. Soil Biology and Biochemistry, 43, 1333–1340. Hodkinson ID, Webb NR, Coulson SJ (2002) Primary community assembly on land – the missing stages: why are the heterotrophic organisms always first? Journal of Ecology, 90, 569–577. Jenny H (1980) Soil Genesis with Ecological Perspectives. Springer-Verlag, New York. Jumpponen A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytologist, 158, 569–578. Kennedy PG, Bruns TD (2005) Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytologist, 166, 631–638. Knelman JE, Legg TM, O’Neill SP et al. (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biology & Biochemistry, 46, 172–180. Miller RM (1979) Some occurrences of vesicular arbuscular mycorrhiza in natural and disturbed ecosystems of the Red Desert. Canadian Journal of Botany, 57, 619–623. Mladenov N, Williams MW, Schmidt SK, Cawley K (2012) Atmospheric deposition as a source of carbon and nutrients to an alpine catchment of the Colorado Rocky Mountains. Biogeosciences, 9, 3337–3355. Naff CS, Darcy JL, Schmidt SK (2013) Phylogeny and biogeography of an uncultured clade of Snow Chytrids. Environmental Microbiology, 15, 2672–2680. Nemergut DR, Anderson SP, Cleveland CC et al. (2007) Microbial community succession in unvegetated, recently-deglaciated soils. Microbial Ecology, 53, 110–122. Nemergut DR, Schmidt SK, Fukami T et al. (2013) Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews, 77, 342–356. Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proceedings. Biological sciences/The Royal Society, 279, 749–758. Sattin SR, Cleveland CC, Hood E et al. (2009) Functional shifts in unvegetated, perhumid, recently deglaciated soils do not
258 N E W S A N D V I E W S : P E R S P E C T I V E correlate with shifts in soil bacterial community composition. Journal of Microbiology, 47, 673–681. Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA et al. (2008a) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and Rocky Mountains. Arctic, Antarctic, and Alpine Research, 40, 576–583. Schmidt SK, Reed SC, Nemergut DR et al. (2008b) The earliest stages of ecosystem succession in high-elevation, recently de-glaciated soils. Proceedings. Biological sciences/The Royal Society, 275, 2793–2802. Schmidt SK, Nemergut DR, Miller AE et al. (2009) Microbial activity and diversity during extreme freeze-thaw cycles in periglacial soils, 5400 m elevation, Cordillera Vilcanota, Per u. Extremophiles, 13, 807–816. Schmidt SK, Lynch RC, King AJ et al. (2011) Phylogeography of microbial phototrophs in the dry valleys of the high Himalayas and Antarctica. Proceedings. Biological sciences/The Royal Society, 278, 702–708. Schmidt SK, Nemergut DR, Todd BT et al. (2012) A simple method for determining limiting nutrients for photosynthetic crusts. Plant Ecology & Diversity, 5, 513–519. Swan LW (1992) The aeolian biome, ecosystems of the Earth’s extremes. BioScience, 42, 262–270.
Vellend M (2010) Conceptual synthesis in community ecology. Review Literature and Arts of the Americas, 85, 183–206. Welker JM, Fahnestock JT, Henry GHR, O’Dea KW, Piper RE (2002) Microbial activity discovered in previously ice-entombed Arctic ecosystems. EOS Transactions American Geophysical Union, 83, 281–284. Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I (2012) Modeling the effect of size on the aerial dispersal of microorganisms. Journal of Biogeography, 39, 89–97. Yoshitake S, Uchida M, Koizumi H, Nakatsubo T (2007) Carbon and nitrogen limitation of soil microbial respiration in high Arc tic successional glacier foreland near Ny-Alesund, Svalbard. Polar Research, 26, 22–30. Zumsteg A, Luster J, G€ oransson H et al. (2012) Bacterial, archaeal and fungal succession in the forefield of a receding glacier. Microbial Ecology, 63, 552–564.
S.S., D.N., J.D. and R.L. wrote the paper. doi: 10.1111/mec.12589
© 2013 John Wiley & Sons Ltd
NEWS AND VIEWS
PERSPECTIVE
Do bacterial and fungal communities assemble differently during primary succession? S. K. SCHMIDT,* D. R. NEMERGUT,†‡ J . L . D A R C Y * and R . L Y N C H * *Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA; †Institute of Arctic and Alpine Research, University of Colorado, Boulder, CO 80309, USA; ‡Environmental Studies Program, University of Colorado, Boulder, CO 80309, USA
High-throughput sequencing technologies are now allowing us to study patterns of community assembly for diverse microbial assemblages across environmental gradients 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-successional 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 succession. We especially need a better understanding of global and regional patterns of microbial dispersal and what environmental factors control the development of microbial communities in complex natural systems. Keywords: bacteria, climate change, community ecology, fungi, landscape genetics, phylogeography Received 24 October 2013; revised 2013
xxxx; accepted 12 November
The conceptual framework for understanding primary succession was initially developed from the study of plant Correspondence: Steve Schmidt, Fax: 303-492-8699; E-mail: [email protected]
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 generalized community assembly theory (Vellend 2010; Nemergut 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 profiles 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 chronosequence 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 trajectories 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 discuss the results of Brown & Jumpponen (2014) from the perspective of this debate and with respect to the growing body of knowledge about microbial dispersal, biogeography and biogeochemistry. Perhaps the most interesting finding of Brown & Jumpponen (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 communities were more affected by both distance along the chronosequence 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 deterministic) 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 of
© 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 255 Fig. 1 Repeat photography of a site in the High Andes of Per u where rapid glacial 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 person 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 person 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.
succession for bacteria and fungi at this site. If bacterial communities converge on one community type during succession, 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-successional Betaproteobacteria (e.g. Polaromonas spp.) are not dispersal 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). © 2013 John Wiley & Sons Ltd
Recent modelling studies also support a difference in dispersal 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 & Jumpponen 2014) of bacteria at early-successional sites (Fig. 2). A more consistent propagule rain for bacteria could reduce or eliminate priority effects for bacterial communities resulting in more deterministic community assembly across the landscape compared with fungi. Other research
256 N E W S A N D V I E W S : P E R S P E C T I V E
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 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.
has shown that priority effects can lead to greater divergence 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 determined 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 successional 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 exhibit a broader range of physiologies than do fungi and thus are more likely to be successful colonists of the oligotrophic, plant-free soils near the glacier terminus. Earlysuccessional bacteria can be photoautotrophs, heterotrophs or chemoautotrophs and many can fix atmospheric nitrogen (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 originally 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 stochastic) accumulation of organic matter (and therefore fungi) across the early-successional landscape. Brown & Jumpponen (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 autochthonously 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 earlysuccessional soils probably has a major effect on the structure 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 limitations of essential nutrients (Yoshitake et al. 2007; G€ oransson 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 geochemistry and aeolian inputs of nutrients to all of the earlysuccessional sites presently being studied by microbial ecologists (Mladenov et al. 2012). Finally, the relationship between plant and soil microbial communities in early-successional sites should be highly correlated (Blaalid et al. 2012; Knelman et al. 2012) as the nutrient cycling cascades catalysed by microorganisms in plant-free soils are likely to strongly influence the success of plant colonization and because plants add substantial inputs of carbon to the soils through both litter and root exudates. Most importantly, plants form symbiotic relationships with many soil bacteria and fungi and should therefore skew microbial community assembly towards symbiotic heterotrophs. Therefore, it was somewhat 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 bacteria as discussed above. Previous studies have shown that inoculum levels for the most common type of plant
© 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 257 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 difference in patterns of bacterial distribution along the chronosequence. 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 deterministic 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. Especially needed are studies of the relative dispersal abilities of microbial groups and studies of nutrient levels, inputs and limitations in early-successional systems. New, highthroughput sequencing technologies have allowed us to finally describe the spatial and temporal patterns of microbial communities, but mechanistic studies that isolate the relative importance of the individual drivers of microbial community assembly lag far behind.
References Bardgett RD, Richter A, Bol R et al. (2007) Heterotrophic microbial communities use ancient carbon following glacial retreat. Biology Letters, 3, 487–490. Blaalid R, Carlsen T, Kumar S et al. (2012) Changes in root-associated fungal communities along a primary succession gradient analyzed by 454 pyrosequencing. Molecular Ecology, 21, 1897– 1908. Brown SP, Jumpponen A (2014) Contrasting primary successional trajectories of fungi and bacteria in retreating glacier soils. Molecular Ecology, 23, 481–497. Chase JM (2003) Community assembly: when should history matter? Oecologia, 136, 489–498. Clements FE (1916) Plant Succession: An Analysis of the Development of Vegetation (No. 242). Carnegie Institution of Washington, Washington, DC.
© 2013 John Wiley & Sons Ltd
Clements FE (1936) Nature and structure of the climax. Journal of Ecology, 24, 252–284. Darcy JL, Lynch RC, King AJ, Robeson MS, Schmidt SK (2011) Global distribution of Polaromonas phylotypes - evidence for a highly successful dispersal capacity. PLoS ONE, 6, e23742. doi:10.1371/ journal.pone.0023742. De Wever A, Leliaert F, Verleyen E et al. (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proceedings. Biological sciences/The Royal Society, 276, 3591–3599. Duc L, Noll M, Meier BE, B€ urgmann H, Zeyer J (2009) High diversity of diazotrophs in the forefield of a receding Alpine glacier. Microbial Ecology, 57, 179–190. Ferrenberg S, O’Neill SP, Knelman JE et al. (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. The ISME Journal, 7, 1102–1111. Fierer N, Nemergut D, Knight R, Craine JM (2010) Changes through time: integrating microorganisms into the study of succession. Research in Microbiology, 161, 635–642. Fukami T, Dickie IA, Wilkie JP et al. (2010) Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecology Letters, 13, 675–684. Gleason HA (1926) The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club, 53, 7–26. G€ oransson H, Venterink HO, B a ath E (2011) Soil bacterial growth and nutrient limitation along a chronosequence from a glacier forefield. Soil Biology and Biochemistry, 43, 1333–1340. Hodkinson ID, Webb NR, Coulson SJ (2002) Primary community assembly on land – the missing stages: why are the heterotrophic organisms always first? Journal of Ecology, 90, 569–577. Jenny H (1980) Soil Genesis with Ecological Perspectives. Springer-Verlag, New York. Jumpponen A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytologist, 158, 569–578. Kennedy PG, Bruns TD (2005) Priority effects determine the outcome of ectomycorrhizal competition between two Rhizopogon species colonizing Pinus muricata seedlings. New Phytologist, 166, 631–638. Knelman JE, Legg TM, O’Neill SP et al. (2012) Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biology & Biochemistry, 46, 172–180. Miller RM (1979) Some occurrences of vesicular arbuscular mycorrhiza in natural and disturbed ecosystems of the Red Desert. Canadian Journal of Botany, 57, 619–623. Mladenov N, Williams MW, Schmidt SK, Cawley K (2012) Atmospheric deposition as a source of carbon and nutrients to an alpine catchment of the Colorado Rocky Mountains. Biogeosciences, 9, 3337–3355. Naff CS, Darcy JL, Schmidt SK (2013) Phylogeny and biogeography of an uncultured clade of Snow Chytrids. Environmental Microbiology, 15, 2672–2680. Nemergut DR, Anderson SP, Cleveland CC et al. (2007) Microbial community succession in unvegetated, recently-deglaciated soils. Microbial Ecology, 53, 110–122. Nemergut DR, Schmidt SK, Fukami T et al. (2013) Patterns and processes of microbial community assembly. Microbiology and Molecular Biology Reviews, 77, 342–356. Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. Proceedings. Biological sciences/The Royal Society, 279, 749–758. Sattin SR, Cleveland CC, Hood E et al. (2009) Functional shifts in unvegetated, perhumid, recently deglaciated soils do not
258 N E W S A N D V I E W S : P E R S P E C T I V E correlate with shifts in soil bacterial community composition. Journal of Microbiology, 47, 673–681. Schmidt SK, Sobieniak-Wiseman LC, Kageyama SA et al. (2008a) Mycorrhizal and dark-septate fungi in plant roots above 4270 meters elevation in the Andes and Rocky Mountains. Arctic, Antarctic, and Alpine Research, 40, 576–583. Schmidt SK, Reed SC, Nemergut DR et al. (2008b) The earliest stages of ecosystem succession in high-elevation, recently de-glaciated soils. Proceedings. Biological sciences/The Royal Society, 275, 2793–2802. Schmidt SK, Nemergut DR, Miller AE et al. (2009) Microbial activity and diversity during extreme freeze-thaw cycles in periglacial soils, 5400 m elevation, Cordillera Vilcanota, Per u. Extremophiles, 13, 807–816. Schmidt SK, Lynch RC, King AJ et al. (2011) Phylogeography of microbial phototrophs in the dry valleys of the high Himalayas and Antarctica. Proceedings. Biological sciences/The Royal Society, 278, 702–708. Schmidt SK, Nemergut DR, Todd BT et al. (2012) A simple method for determining limiting nutrients for photosynthetic crusts. Plant Ecology & Diversity, 5, 513–519. Swan LW (1992) The aeolian biome, ecosystems of the Earth’s extremes. BioScience, 42, 262–270.
Vellend M (2010) Conceptual synthesis in community ecology. Review Literature and Arts of the Americas, 85, 183–206. Welker JM, Fahnestock JT, Henry GHR, O’Dea KW, Piper RE (2002) Microbial activity discovered in previously ice-entombed Arctic ecosystems. EOS Transactions American Geophysical Union, 83, 281–284. Wilkinson DM, Koumoutsaris S, Mitchell EAD, Bey I (2012) Modeling the effect of size on the aerial dispersal of microorganisms. Journal of Biogeography, 39, 89–97. Yoshitake S, Uchida M, Koizumi H, Nakatsubo T (2007) Carbon and nitrogen limitation of soil microbial respiration in high Arc tic successional glacier foreland near Ny-Alesund, Svalbard. Polar Research, 26, 22–30. Zumsteg A, Luster J, G€ oransson H et al. (2012) Bacterial, archaeal and fungal succession in the forefield of a receding glacier. Microbial Ecology, 63, 552–564.
S.S., D.N., J.D. and R.L. wrote the paper. doi: 10.1111/mec.12589
© 2013 John Wiley & Sons Ltd
