Stochastic and deterministic assembly processes in subsurface microbial communities

ISME Journal - Tập 6 Số 9 - Trang 1653-1664 - 2012
James Stegen1, Xueju Lin2,3, Allan Konopka3, James K. Fredrickson3
1Fundamental and Computational Sciences Directorate, Biological Sciences Division, Pacific Northwest National Laboratory, Richland, WA 99352, USA.
22Current address: School of Biology, Georgia Institute of Technology, Atlanta, GA 30332, USA.,
3Fundamental and Computational Sciences Directorate, Biological Sciences Division, Pacific Northwest National Laboratory , Richland, WA , USA

Tóm tắt

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.

Từ khóa


Tài liệu tham khảo

Amaral-Zettler, 2011, Microbial community structure across the tree of life in the extreme Rio Tinto, ISME J, 5, 42, 10.1038/ismej.2010.101

Andersson, 2010, Pyrosequencing reveals contrasting seasonal dynamics of taxa within Baltic Sea bacterioplankton communities, ISME J, 4, 171, 10.1038/ismej.2009.108

Bjornstad, 2009, Borehole Completion and Conceptual Hydrogeologic Model for the IFRC Well Field, 300 Area, Hanford Site, 10.2172/974984

Bork, 2009, Quantifying environmental adaptation of metabolic pathways in metagenomics, Proc Natl Acad Sci USA, 106, 1374, 10.1073/pnas.0808022106

Bryant, 2008, Microbes on mountainsides: contrasting elevational patterns of bacterial and plant diversity, Proc Natl Acad Sci USA, 105, 11505, 10.1073/pnas.0801920105

Caporaso, 2010, QIIME allows analysis of high-throughput community sequencing data, Nat Methods, 7, 335, 10.1038/nmeth.f.303

Caruso, 2011, Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale, ISME J, 5, 1406, 10.1038/ismej.2011.21

Chase, 2007, Drought mediates the importance of stochastic community assembly, Proc Natl Acad Sci, 104, 17430, 10.1073/pnas.0704350104

Chase, 2010, Stochastic community assembly causes higher biodiversity in more productive environments, Science, 328, 1388, 10.1126/science.1187820

Chase, 2009, Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities, Ecol Lett, 12, 1210, 10.1111/j.1461-0248.2009.01362.x

Chase, 2011, Using null models to disentangle variation in community dissimilarity from variation in α-diversity, Ecosphere, 2, Art24, 10.1890/ES10-00117.1

Chase, 2011, Disentangling the importance of ecological niches from stochastic processes across scales, Philos Trans R Soc B: Biol Sci, 366, 2351, 10.1098/rstb.2011.0063

Chesson, 2000, Mechanisms of maintenance of species diversity, Annu Rev Ecol Syst, 31, 343, 10.1146/annurev.ecolsys.31.1.343

Clements, 1916, Plant Succession

Cohan, 2008, The origins of ecological diversity in prokaryotes, Curr Biol, 18, R1024, 10.1016/j.cub.2008.09.014

Costello, 2009, Fumarole-supported Islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes, Appl Environ Microb, 75, 735, 10.1128/AEM.01469-08

Diamond, 1975, Ecol Evol Communities

Diniz-Filho, 2010, Hidden patterns of phylogenetic non-stationarity overwhelm comparative analyses of niche conservatism and divergence, Global Ecol Biogeogr, 19, 916, 10.1111/j.1466-8238.2010.00562.x

Doolittle, 1999, Lateral genomics, Trends Biochem Sci, 24, M5, 10.1016/S0968-0004(99)01471-1

Doolittle, 1999, Phylogenetic classification and the universal tree, Science, 284, 2124, 10.1126/science.284.5423.2124

Dumbrell, 2010, Relative roles of niche and neutral processes in structuring a soil microbial community, ISME J, 4, 337, 10.1038/ismej.2009.122

Fierer, 2007, Toward an ecological classification of soil bacteria, Ecology, 88, 1354, 10.1890/05-1839

Fierer, 2008, The influence of sex, handedness, and washing on the diversity of hand surface bacteria, Proc Natl Acad Sci USA, 105, 17994, 10.1073/pnas.0807920105

Fine, 2011, Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities, Ecography, 34, 552, 10.1111/j.1600-0587.2010.06548.x

Fuhrman, 2006, Annually reoccurring bacterial communities are predictable from ocean conditions, Proc Natl Acad Sci USA, 103, 13104, 10.1073/pnas.0602399103

Gerisch, 2011, More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity, Oikos, 121, 508, 10.1111/j.1600-0706.2011.19749.x

Gilbert, 2012, Defining seasonal marine microbial community dynamics, ISME J, 6, 298, 10.1038/ismej.2011.107

Gleason, 1927, Further views on the succession concept, Ecology, 8, 299, 10.2307/1929332

Graham, 2008, Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time, Ecol Lett, 11, 1265, 10.1111/j.1461-0248.2008.01256.x

Haldane, 1932, The Causes of Evolution

Herrera, 2010, Inhospitable sweetness: nectar filtering of pollinator-borne inocula leads to impoverished, phylogenetically clustered yeast communities, Proc R Soc B-Biol Sci, 277, 747, 10.1098/rspb.2009.1485

Horner-Devine, 2006, Phylogenetic clustering and overdispersion in bacterial communities, Ecology, 87, 100, 10.1890/0012-9658(2006)87[100:PCAOIB]2.0.CO;2

Hubbell, 2001, The Unified Neutral Theory of Biodiversity and Biogeography

Jones, 2010, Ecological and evolutionary factors underlying global and local assembly of denitrifier communities, ISME J, 4, 633, 10.1038/ismej.2009.152

Kembel, 2009, Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests, Ecol Lett, 12, 949, 10.1111/j.1461-0248.2009.01354.x

Kembel, 2011, The phylogenetic diversity of metagenomes, Plos One, 6, e23214, 10.1371/journal.pone.0023214

Knight, 2005, UniFrac: a new phylogenetic method for comparing microbial communities, Appl Environ Microb, 71, 8228, 10.1128/AEM.71.12.8228-8235.2005

Kraft, 2007, Trait evolution, community assembly, and the phylogenetic structure of ecological communities, Am Nat, 170, 271, 10.1086/519400

Langenheder, 2011, Species sorting and neutral processes are both important during the initial assembly of bacterial communities, ISME J, 5, 1086, 10.1038/ismej.2010.207

Losos, 2008, Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species, Ecol Lett, 11, 995, 10.1111/j.1461-0248.2008.01229.x

Myers, 2009, Local immigration, competition from dominant guilds, and the ecological assembly of high-diversity pine savannas, Ecology, 90, 2745, 10.1890/08-1953.1

Myers, 2010, Seed arrival and ecological filters interact to assemble high-diversity plant communities, Ecology, 92, 676, 10.1890/10-1001.1

Ofiteru, 2010, Combined niche and neutral effects in a microbial wastewater treatment community, Proc Natl Acad Sci USA, 107, 15345, 10.1073/pnas.1000604107

Pei, 2011, Exploring tree-habitat associations in a chinese subtropical forest plot using a molecular phylogeny generated from DNA Barcode Loci, Plos One, 6, e21273, 10.1371/journal.pone.0021273

Philippot, 2010, The ecological coherence of high bacterial taxonomic ranks, Nat Rev Micro, 8, 523, 10.1038/nrmicro2367

Schwarz, 1978, Estimating the dimension of a model, Annals Stat, 6, 461, 10.1214/aos/1176344136

Sun, 2006, Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors, Bioinformatics, 22, 2532, 10.1093/bioinformatics/btl503

Vamosi, 2009, Emerging patterns in the comparative analysis of phylogenetic community structure, Mol Ecol, 18, 572, 10.1111/j.1365-294X.2008.04001.x

Vellend, 2010, Conceptual synthesis in community ecology, Q Rev Biol, 85, 183, 10.1086/652373

Vermeul, 2011, River-induced flow dynamics in long-screen wells and impact on aqueous samples, Ground Water, 49, 515, 10.1111/j.1745-6584.2010.00769.x

Webb, 2000, Exploring the phylogenetic structure of ecological communities: An example for rain forest trees, Am Nat, 156, 145, 10.1086/303378

Webb, 2002, Phylogenies and community ecology, Annu Rev Ecol Syst, 33, 475, 10.1146/annurev.ecolsys.33.010802.150448

Weiher, 2011, Advances, challenges and a developing synthesis of ecological community assembly theory, Philos Trans R Soc B: Biol Sci, 366, 2403, 10.1098/rstb.2011.0056

Weiher, 1995, Assembly rules, null models, and trait dispersion: New questions from old patterns, Oikos, 74, 159, 10.2307/3545686

Welch, 2002, Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli, Proc Natl Acad Sci USA, 99, 17020, 10.1073/pnas.252529799

Wiedenbeck, 2011, Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches, FEMS Microbiol Rev, 35, 957, 10.1111/j.1574-6976.2011.00292.x

Zinger, 2011, Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems, Plos One, 6, e24570, 10.1371/journal.pone.0024570