Abstract
A major goal of microbial community ecology is to understand the forces that structure community composition. Deterministic selection by specific environmental factors is sometimes important, but in other cases stochastic or ecologically neutral processes dominate. Lacking is a unified conceptual framework aiming to understand why deterministic processes dominate in some contexts but not others. Here we work toward such a framework. By testing predictions derived from general ecological theory we aim to uncover factors that govern the relative influences of deterministic and stochastic processes. We couple spatiotemporal data on subsurface microbial communities and environmental parameters with metrics and null models of within and between community phylogenetic composition. Testing for phylogenetic signal in organismal niches showed that more closely related taxa have more similar habitat associations. Community phylogenetic analyses further showed that ecologically similar taxa coexist to a greater degree than expected by chance. Environmental filtering thus deterministically governs subsurface microbial community composition. More importantly, the influence of deterministic environmental filtering relative to stochastic factors was maximized at both ends of an environmental variation gradient. A stronger role of stochastic factors was, however, supported through analyses of phylogenetic temporal turnover. Although phylogenetic turnover was on average faster than expected, most pairwise comparisons were not themselves significantly non-random. The relative influence of deterministic environmental filtering over community dynamics was elevated, however, in the most temporally and spatially variable environments. Our results point to general rules governing the relative influences of stochastic and deterministic processes across micro- and macro-organisms.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Amaral-Zettler LA, Zettler ER, Theroux SM, Palacios C, Aguilera A, Amils R . 2011. Microbial community structure across the tree of life in the extreme Rio Tinto. ISME J 5: 42–50.
Andersson AF, Riemann L, Bertilsson S . 2010. Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities. ISME J 4: 171–181.
Bjornstad BN, Horner JA, Vermeul VR, Lanigan DC, Thorne PD . 2009 Borehole Completion and Conceptual Hydrogeologic Model for the IFRC Well Field, 300 Area, Hanford Site. PNNL-18340, Pacific Northwest National Laboratory, Richland, WA.
Bork P, Gianoulis TA, Raes J, Patel PV, Bjornson R, Korbel JO et al. 2009. Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc Natl Acad Sci USA 106: 1374–1379.
Bryant JA, Lamanna C, Morlon H, Kerkhoff AJ, Enquist BJ, Green JL . 2008. Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity. Proc Natl Acad Sci USA 105: 11505–11511.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336.
Caruso T, Chan YK, Lacap DC, Lau MCY, Mckay CP, Pointing SB . 2011. Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME J 5: 1406–1413.
Chase JM . 2007. Drought mediates the importance of stochastic community assembly. Proc Natl Acad Sci 104: 17430–17434.
Chase JM . 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328: 1388–1391.
Chase JM, Biro EG, Ryberg WA, Smith KG . 2009. Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecol Lett 12: 1210–1218.
Chase JM, Kraft NJB, Smith KG, Vellend M, Inouye BD . 2011. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2: Art24.
Chase JM, Myers JA . 2011. Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc B: Biol Sci 366: 2351–2363.
Chesson P . 2000. Mechanisms of maintenance of species diversity. Annu Rev Ecol Syst 31: 343–366.
Clements FE . 1916 Plant Succession. Carnegie Institution of Washington, Washington, DC.
Cohan FM, Koeppel AF . 2008. The origins of ecological diversity in prokaryotes. Curr Biol 18: R1024–U1017.
Costello EK, Halloy SRP, Reed SC, Sowell P, Schmidt SK . 2009. Fumarole-supported Islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes. Appl Environ Microb 75: 735–747.
Diamond JM . 1975. Assembly of species communities. In: ML Cody, JM Diamond (eds) Ecol Evol Communities. Harvard University Press, Cambridge, MA.
Diniz-Filho JAF, Terribile LC, da Cruz MJR, Vieira LCG . 2010. Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence. Global Ecol Biogeogr 19: 916–926.
Doolittle WF . 1999a. Lateral genomics. Trends Biochem Sci 24: M5–M8.
Doolittle WF . 1999b. Phylogenetic classification and the universal tree. Science 284: 2124–2128.
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH . 2010. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4: 337–345.
Fierer N, Bradford MA, Jackson RB . 2007. Toward an ecological classification of soil bacteria. Ecology 88: 1354–1364.
Fierer N, Hamady M, Lauber CL, Knight R . 2008. The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci USA 105: 17994–17999.
Fine PVA, Kembel SW . 2011. Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography 34: 552–565.
Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S . 2006. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA 103: 13104–13109.
Gerisch M, Agostinelli V, Henle K, Dziock F . 2011. More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity. Oikos 121: 508–515.
Gilbert JA, Steele JA, Caporaso JG, Steinbruck L, Reeder J, Temperton B et al. 2012. Defining seasonal marine microbial community dynamics. ISME J 6: 298–308.
Gleason HA . 1927. Further views on the succession concept. Ecology 8: 299–326.
Graham CH, Fine PVA . 2008. Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecol Lett 11: 1265–1277.
Haldane JBS . 1932 The Causes of Evolution. Longmans, Green and Company, London, UK.
Hardy OJ, Couteron P, Munoz F, Ramesh BR, Pélissier R . 2012. Phylogenetic turnover in tropical tree communities: impact of environmental filtering, biogeography and mesoclimatic niche conservatism. Global Ecol Biogeogr doi:10.1111/j.1466-8238.2011.00742.x.
Herrera CM, Canto A, Pozo MI, Bazaga P . 2010. Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities. Proc R Soc B-Biol Sci 277: 747–754.
Horner-Devine MC, Bohannan BJM . 2006. Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87: 100–108.
Hubbell SP . 2001 The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princeton, NJ.
Jones CM, Hallin S . 2010. Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4: 633–641.
Kembel SW . 2009. Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12: 949–960.
Kembel SW, Eisen JA, Pollard KS, Green JL . 2011. The phylogenetic diversity of metagenomes. Plos One 6: e23214.
Knight R, Lozupone C . 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microb 71: 8228–8235.
Kraft NJB, Cornwell WK, Webb CO, Ackerly DD . 2007. Trait evolution, community assembly, and the phylogenetic structure of ecological communities. Am Nat 170: 271–283.
Langenheder S, Szekely AJ . 2011. Species sorting and neutral processes are both important during the initial assembly of bacterial communities. ISME J 5: 1086–1094.
Lin X, Mckinley J, Resch CT, Lauber C, Fredrickson J, Konopka AE . 2012. Spatial and temporal dynamics of microbial community in the Hanford unconfined aquifer. ISME J e-pub ahead of print 29 March 2012; doi:10.1038/ismej.2012.26.
Losos JB . 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11: 995–1003.
McKinley JP, Zachara JM, Resch CT, Kaluzny RM, Miller MD, Vermeul VR et al. (in review) River water intrusion and contaminant uranium contributions from the vadose zone to groundwater during the annual Spring rise in Columbia River stage at the Hanford Site, Washington. Environ Sci Technol.
Myers JA, Harms KE . 2009. Local immigration, competition from dominant guilds, and the ecological assembly of high-diversity pine savannas. Ecology 90: 2745–2754.
Myers JA, Harms KE . 2010. Seed arrival and ecological filters interact to assemble high-diversity plant communities. Ecology 92: 676–686.
Ofiteru ID, Lunn M, Curtis TP, Wells GF, Criddle CS, Francis CA et al. 2010. Combined niche and neutral effects in a microbial wastewater treatment community. Proc Natl Acad Sci USA 107: 15345–15350.
Pei NC, Lian JY, Erickson DL, Swenson NG, Kress WJ, Ye WH et al. 2011. Exploring tree-habitat associations in a chinese subtropical forest plot using a molecular phylogeny generated from DNA Barcode Loci. Plos One 6: e21273.
Philippot L, Andersson SGE, Battin TJ, Prosser JI, Schimel JP, Whitman WB et al. 2010. The ecological coherence of high bacterial taxonomic ranks. Nat Rev Micro 8: 523–529.
Schwarz G . 1978. Estimating the dimension of a model. Annals Stat 6: 461–464.
Sun FZ, Ruan QS, Dutta D, Schwalbach MS, Steele JA, Fuhrman JA . 2006. Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics 22: 2532–2538.
Vamosi SM, Heard SB, Vamosi JC, Webb CO . 2009. Emerging patterns in the comparative analysis of phylogenetic community structure. Mol Ecol 18: 572–592.
van der Plas F, Anderson TM, Olff H . 2012. Trait similarity patterns within grass and grasshopper communities: multitrophic community assembly at work. Ecology doi:10.1890/11-0975.1.
Vellend M . 2010. Conceptual synthesis in community ecology. Q Rev Biol 85: 183–206.
Vermeul VR, McKinley JP, Newcomer DR, Mackley RD, Zachara JM . 2011. River-induced flow dynamics in long-screen wells and impact on aqueous samples. Ground Water 49: 515–524.
Webb CO . 2000. Exploring the phylogenetic structure of ecological communities: An example for rain forest trees. Am Nat 156: 145–155.
Webb CO, Ackerly DD, Kembel S . 2011, Phylocom: Software for the analysis of phylogenetic community structure and character evolution (with phylomatic and ecoevolve). User's manual, version 4.2. http://www.phylodiversity.net/phylocom/.
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ . 2002. Phylogenies and community ecology. Annu Rev Ecol Syst 33: 475–505.
Weiher E, Freund D, Bunton T, Stefanski A, Lee T, Bentivenga S . 2011. Advances, challenges and a developing synthesis of ecological community assembly theory. Philos Trans R Soc B: Biol Sci 366: 2403–2413.
Weiher E, Keddy P . 1995. Assembly rules, null models, and trait dispersion: New questions from old patterns. Oikos 74: 159–164.
Welch RA, Burland V, Plunkett G, Redford P, Roesch P, Rasko D et al. 2002. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 99: 17020–17024.
Wiedenbeck J, Cohan FM . 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35: 957–976.
Zinger L, Amaral-Zettler LA, Fuhrman JA, Horner-Devine MC, Huse SM, Welch DBM et al. 2011. Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems. Plos One 6: e24570.
Acknowledgements
JCS was supported by a Linus Pauling Distinguished Postdoctoral Fellowship at Pacific Northwest National Laboratory. We thank NG Swenson for helpful discussions on quantifying phylogenetic signal and on a previous version of the manuscript. This research was supported by the U.S. Department of Energy (DOE), Office of Biological and Environmental Research(BER), as part of Subsurface Biogeochemistry Research Program’s Scientific Focus Area (SFA) and Integrated Field-Scale Research Challenge (IFRC) at the Pacific Northwest National Laboratory (PNNL). PNNL is operated for DOE by Battelle under contract DE-AC06–76RLO 1830.
Author information
Authors and Affiliations
Corresponding author
Additional information
Supplementary Information accompanies the paper on The ISME Journal website
Supplementary information
Rights and permissions
About this article
Cite this article
Stegen, J., Lin, X., Konopka, A. et al. Stochastic and deterministic assembly processes in subsurface microbial communities. ISME J 6, 1653–1664 (2012). https://doi.org/10.1038/ismej.2012.22
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/ismej.2012.22
Keywords
This article is cited by
-
Taxonomic dependency and spatial heterogeneity in assembly mechanisms of bacteria across complex coastal waters
Ecological Processes (2024)
-
Environmental stress mediates groundwater microbial community assembly
Nature Microbiology (2024)
-
Resilience of anodic biofilm in microbial fuel cell biosensor for BOD monitoring of urban wastewater
npj Clean Water (2024)
-
Response of particle-attached and free-living bacterial communities to Microcystis blooms
Applied Microbiology and Biotechnology (2024)
-
Nitrogen deposition mediates more stochastic processes in structuring plant community than soil microbial community in the Eurasian steppe
Science China Life Sciences (2024)
