Skip to main content
Log in

Assembly mechanisms of soil bacterial communities in subalpine coniferous forests on the Loess Plateau, China

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Microbial community assembly is affected by trade-offs between deterministic and stochastic processes. However, the mechanisms underlying the relative influences of the two processes remain elusive. This knowledge gap limits our ability to understand the effects of community assembly processes on microbial community structures and functions. To better understand community assembly mechanisms, the community dynamics of bacterial ecological groups were investigated based on niche breadths in 23 soil plots from subalpine coniferous forests on the Loess Plateau in Shanxi, China. Here, the overall community was divided into the ecological groups that corresponded to habitat generalists, ‘other taxa’ and specialists. Redundancy analysis based on Bray-Curtis distances (db-RDA) and multiple regression tree (MRT) analysis indicated that soil organic carbon (SOC) was a general descriptor that encompassed the environmental gradients by which the communities responded to, because it can explain more significant variations in community diversity patterns. The three ecological groups exhibited different niche optima and degrees of specialization (i.e., niche breadths) along the SOC gradient, suggesting the presence of a gradient in tolerance for environmental heterogeneity. The inferred community assembly processes varied along the SOC gradient, wherein a transition was observed from homogenizing dispersal to variable selection that reflects increasing deterministic processes. Moreover, the ecological groups were inferred to perform different community functions that varied with community composition, structure. In conclusion, these results contribute to our understanding of the trade-offs between community assembly mechanisms and the responses of community structure and function to environmental gradients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barberán, A., Bates, S.T., Casamayor, E.O., and Fierer, N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J. 6, 343–351.

    Article  CAS  PubMed  Google Scholar 

  • Bastida, F., Torres, I.F., Hernández, T., Bombach, P., Richnow, H.H., and García, C. 2013. Can the labile carbon contribute to carbon immobilization in semiarid soils? Priming effects and microbial community dynamics. Soil Biol. Biochem. 57, 892–902.

    Article  CAS  Google Scholar 

  • Bulgarelli, D., Garrido-Oter, R., Münch, P.C., Weiman, A., Dröge, J., Pan, Y., McHardy, A.C., and Schulze-Lefert, P. 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17, 392–403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chase, J.M. and Myers, J.A. 2011. Disentangling the importance of ecological niches from stochastic processes across scales. Philos T. R. Soc. B 366, 2351–2363.

    Article  Google Scholar 

  • Chisholm, R.A. and Pacala, S.W. 2011. Theory predicts a rapid transition from niche-structured to neutral biodiversity patterns across a speciation-rate gradient. Theor. Ecol. 4, 195–200.

    Article  Google Scholar 

  • Condit, R., Pitman, N., Leigh, E.G., Chave, J., Terborgh, J., Foster, R.B., Núñez, P., Aguilar, S., Valencia, R., and Villa, G. 2002. Beta-diversity in tropical forest trees. Science 295, 666–669.

    Article  CAS  PubMed  Google Scholar 

  • Dias, P.C. 1996. Sources and sinks in population biology. Trends Ecol. Evol. 11, 326–330.

    Article  CAS  PubMed  Google Scholar 

  • Dini-Andreote, F., Stegen, J.C., van Elsas, J.D., and Salles, J.F. 2015. Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl. Acad. Sci. USA 112, 1326–1332.

    Article  CAS  Google Scholar 

  • Dumbrell, A.J., Nelson, M., Helgason, T., Dytham, C., and Fitter, A.H. 2010. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J. 4, 337–345.

    Article  PubMed  Google Scholar 

  • Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. 2011. Uchime improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fine, P.V.A. and Kembel, S.W. 2011. Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34, 552–565.

    Article  Google Scholar 

  • Fodelianakis, S., Moustakas, A., Papageorgiou, N., Manoli, O., Tsikopoulou, I., Michoud, G., Daffonchio, D., Karakassis, I., and Ladoukakis, E.D. 2016. Modified niche optima and breadths explain the historical contingency of bacterial community responses to eutrophication in coastal sediments. Mol. Ecol. 26, 2006–2018.

    Article  PubMed  Google Scholar 

  • Futuyma, D.J. and Moreno, G. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207–233.

    Article  Google Scholar 

  • Gilbert, B. and Levin, S.A. 2004. Neutrality, niches, and dispersal in a temperate forest understory. Proc. Natl. Acad. Sci. USA 101, 7651–7656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gravel, D., Canham, C.D., Beaudet, M., and Messier, C. 2006. Reconciling niche and neutrality: The continuum hypothesis. Ecol. Lett. 9, 399–409.

    Article  PubMed  Google Scholar 

  • Hubbell, S.P. and BordadeAgua, L. 2004. Unified neutral theory of biodiversity and biography: Reply. Ecology 85, 3172–3174.

    Article  Google Scholar 

  • Kolasa, J. and Li, B.L. 2003. Removing the confounding effect of habitat specialization reveals the stabilizing contribution of diversity to species variability. Proc. R. Soc. Lond. B-Biol. Sci. 270 Suppl 2, S198–201.

    Google Scholar 

  • Konstantinidis, K.T. and Tiedje, J.M. 2007. Prokaryotic taxonomy and phylogeny in the genomic era: Advancements and challenges ahead. Curr. Opin. Microbiol. 10, 504–509.

    Article  CAS  PubMed  Google Scholar 

  • Kraft, N.J., Cornwell, W.K., Webb, C.O., and Ackerly, D.D. 2007. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am. Nat. 170, 271–283.

    Article  PubMed  Google Scholar 

  • Leibold, M.A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J.M., Hoopes, M.F., Holt, R.D., Shurin, J.B., Law, R., and Tilman, D. 2010. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601–613.

    Article  Google Scholar 

  • Levins, R. 1968. Evolution in changing environments: Some theoretical explorations. No. 2. Princeton University Press, Princeton, USA.

    Google Scholar 

  • Liao, J., Cao, X., Wang, J., Zhao, L., Sun, J., Jiang, D., and Huang, Y. 2017. Similar community assembly mechanisms underlie similar biogeography of rare and abundant bacteria in lakes on Yungui Plateau, China. Limnol. Oceanogr. 62, 723–735.

    Article  Google Scholar 

  • Liao, J., Cao, X., Zhao, L., Wang, J., Gao, Z., Caiwang, M.C., and Huang, Y. 2016. The importance of neutral and niche processes for bacterial community assembly differs between habitat generalists and specialists. FEMS Microbiol. Ecol. 92, fiw174.

    Article  CAS  PubMed  Google Scholar 

  • Logares, R., Lindstrom, E.S., Langenheder, S., Logue, J.B., Paterson, H., Laybourn-Parry, J., Rengefors, K., Tranvik, L., and Bertilsson, S. 2013. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J. 7, 937–948.

    Article  CAS  PubMed  Google Scholar 

  • Louca, S., Jacques, S.M.S., Pires, A.P.F., Leal, J.S., Srivastava, D.S., Parfrey, L.W., Farjalla, V.F., and Doebeli, M. 2017. High taxonomic variability despite stable functional structure across microbial communities. Nat. Ecol. Evol. 1, 0015.

    Article  Google Scholar 

  • Louca, S., Parfrey, L.W., and Doebeli, M. 2016. Decoupling function and taxonomy in the global ocean microbiome. Science 353, 1272–1277.

    Article  CAS  PubMed  Google Scholar 

  • Ma, B., Wang, H., Dsouza, M., Lou, J., He, Y., Dai, Z., Brookes, P.C., Xu, J., and Gilbert, J.A. 2016. Geographic patterns of co-occurrence network topological features for soil microbiota at continental scale in Eastern China. ISME J. 10, 1891–1901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Massana, R. and Logares, R. 2013. Eukaryotic versus prokaryotic marine picoplankton ecology. Environ. Microbiol. 15, 1254–1261.

    Article  PubMed  Google Scholar 

  • Monard, C., Gantner, S., Bertilsson, S., Hallin, S., and Stenlid, J. 2016. Habitat generalists and specialists in microbial communities across a terrestrial-freshwater gradient. Sci. Rep. 6, 37719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ofiţeru, I.D., Lunn, M., Curtis, T.P., Wells, G.F., Criddle, C.S., Francis, C.A., and Sloan, W.T. 2010. Combined niche and neutral effects in a microbial waste water treatment community. Proc. Natl. Acad. Sci. USA 107, 15345–15350.

    Article  PubMed  PubMed Central  Google Scholar 

  • Olivierj, H. 2008. Testing the spatial phylogenetic structure of local communities: Statistical performances of different null models and test statistics on a locally neutral community. J. Ecol. 96, 914–926.

    Article  Google Scholar 

  • Pandit, S.N., Kolasa, J., and Cottenie, K. 2009. Contrasts between habitat generalists and specialists: An empirical extension to the basic metacommunity framework. Ecology 90, 2253–2262.

    Article  PubMed  Google Scholar 

  • Pruesse, E., Quast, C., Knittel, K., Fuchs, B.M., Ludwig, W., Peplies, J., and Glöckner, F.O. 2007. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188–7196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reeder, J. and Knight, R. 2010. Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat. Methods 7, 668–669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren, C., Zhang, W., Zhong, Z., Han, X., Yang, G., Feng, Y., and Ren, G. 2017. Differential responses of soil microbial biomass, diversity, and compositions to altitudinal gradients depend on plant and soil characteristics. Sci. Total Environ. 610–611, 750–758.

    PubMed  Google Scholar 

  • Siles, J.A. and Margesin, R. 2016. Abundance and diversity of bacterial, archaeal, and fungal communities along an altitudinal gradient in alpine forest soils: What are the driving factors? Microb. Ecol. 72, 207–220.

    Article  PubMed  PubMed Central  Google Scholar 

  • Siles, J.A. and Margesin, R. 2017. Seasonal soil microbial responses are limited to changes in functionality at two Alpine forest sites differing in altitude and vegetation. Sci. Rep. 7, 2204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stegen, J.C., Lin, X., Fredrickson, J.K., Chen, X., Kennedy, D.W., Murray, C.J., Rockhold, M.L., and Konopka, A. 2013. Quantifying community assembly processes and identifying features that impose them. ISME J. 7, 2069–2079.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stegen, J.C., Lin, X., Fredrickson, J.K., and Konopka, A.E. 2015. Estimating and mapping ecological processes influencing microbial community assembly. Front. Microbiol. 6, 370.

    Article  PubMed  PubMed Central  Google Scholar 

  • Stegen, J.C., Lin, X., Konopka, A.E., and Fredrickson, J.K. 2012. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J. 6, 1653–1664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunagawa, S., Coelho, L.P., Chaffron, S., Kultima, J.R., Labadie, K. Salazar, G., Djahanschiri, B., Zeller, G., Mende, D.R., and Alberti, A. 2015. Ocean plankton. Structure and function of the global ocean microbiome. Science 348, 1261359.

    Article  CAS  PubMed  Google Scholar 

  • Tian, J., Qiao, Y., Wu, B., Chen, H., Li, W., Jiang, N., Zhang, X., and Liu, X. 2017. Ecological succession pattern of fungal community in soil along a retreating glacier. Front. Microbiol. 8, 1028.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tripathi, B.M., Stegen, J.C., Kim, M., Dong, K., Adams, J.M., and Lee, Y.K. 2018. Soil pH mediates the balance between stochastic and deterministic assembly of bacteria. ISME J. 12, 1072–1083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker, C.M., Shoemaker, L.G., Davies, K.F., Nemergut, D.R., and Melbourne, B.A. 2016. Differentiating between niche and neutral assembly in metacommunities using null models of β-diversity. Oikos 125, 778–789.

    Article  Google Scholar 

  • Tuomisto, H., Ruokolainen, K., and Yli-Halla, M. 2003. Dispersal, environment, and floristic variation of western Amazonian forests. Science 299, 241–244.

    Article  CAS  PubMed  Google Scholar 

  • Van Tienderen, P.H. 1991. Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45, 1317–1331.

    Article  PubMed  Google Scholar 

  • Woodcock, S., Van, D.G., Christopher, J., Bell, T., Lunn, M., Curtis, T.P., Head, I.M., and Sloan, W.T. 2007. Neutral assembly of bacterial communities. FEMS Microbiol. Ecol. 62, 171–180.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Z., Yu, G., Zhang, X., Ge, J., He, N., Wang, Q., and Wang, D. 2015. The variations in soil microbial communities, enzyme activities and their relationships with soil organic matter decomposition along the northern slope of Changbai mountain. Appl. Soil Ecol. 86, 19–29.

    Article  Google Scholar 

  • Zhou, J. and Ning, D. 2017. Stochastic community assembly: Does it matter in microbial ecology? Microbiol. Mol. Biol. Rev. 81, e00002–17.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baofeng Chai.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, P., Liu, J., Jia, T. et al. Assembly mechanisms of soil bacterial communities in subalpine coniferous forests on the Loess Plateau, China. J Microbiol. 57, 461–469 (2019). https://doi.org/10.1007/s12275-019-8373-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-019-8373-7

Keywords

Navigation