Neutral and selective dynamics in a synthetic microbial community

Significance We created a synthetic microbial community to help understand how evolution and selection pressure change the species diversity of an ecosystem. Our results show that there is a clear transition between neutral and selective regimes that depends on the rate of immigration as well as the fitness differences. Ecologists debate the relative importance of selective vs. neutral processes in understanding biodiversity. This debate is especially pertinent to microbial communities, which play crucial roles in areas such as health, disease, industry, and the environment. Here, we created a synthetic microbial community using heritable genetic barcodes and tracked community composition over repeated rounds of subculture with immigration. Consistent with theory, we find a transition exists between neutral and selective regimes, and the crossover point depends on the fraction of immigrants and the magnitude of fitness differences. Neutral models predict an increase in diversity with increased carrying capacity, while our selective model predicts a decrease in diversity. The community here lost diversity with an increase in carrying capacity, highlighting that using the correct model is essential for predicting community response to change. Together, these results emphasize the importance of including selection to obtain realistic models of even simple systems.

[1]  Benjamin H. Good,et al.  The Dynamics of Molecular Evolution Over 60,000 Generations , 2017, Nature.

[2]  J. Lennon,et al.  Macroecology for microbiology. , 2017, Environmental microbiology reports.

[3]  Orkun S. Soyer,et al.  Challenges in microbial ecology: building predictive understanding of community function and dynamics , 2016, The ISME Journal.

[4]  Aaron Marc Saunders,et al.  The activated sludge ecosystem contains a core community of abundant organisms , 2015, The ISME Journal.

[5]  James K Fredrickson,et al.  Ecological communities by design , 2015, Science.

[6]  Gavin Sherlock,et al.  Quantitative evolutionary dynamics using high-resolution lineage tracking , 2015, Nature.

[7]  J. Curtis,et al.  Application of a Neutral Community Model To Assess Structuring of the Human Lung Microbiome , 2015, mBio.

[8]  Richard E. Lenski,et al.  Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli , 2014, Science.

[9]  Charles K. Fisher,et al.  The transition between the niche and neutral regimes in ecology , 2013, Proceedings of the National Academy of Sciences.

[10]  Michael J. Wiser,et al.  Long-Term Dynamics of Adaptation in Asexual Populations , 2013, Science.

[11]  M. Cencini,et al.  Species abundances and lifetimes: from neutral to niche-stabilized communities. , 2013, Journal of theoretical biology.

[12]  V. Tremaroli,et al.  Functional interactions between the gut microbiota and host metabolism , 2012, Nature.

[13]  S D Allison,et al.  A trait-based approach for modelling microbial litter decomposition. , 2012, Ecology letters.

[14]  J. Raes,et al.  Microbial interactions: from networks to models , 2012, Nature Reviews Microbiology.

[15]  Nicholas Chia,et al.  Quantification of the relative roles of niche and neutral processes in structuring gastrointestinal microbiomes , 2012, Proceedings of the National Academy of Sciences.

[16]  J. Fuhrman,et al.  Beyond biogeographic patterns: processes shaping the microbial landscape , 2012, Nature Reviews Microbiology.

[17]  Kui Lin,et al.  Coexistence of nearly neutral species , 2012 .

[18]  S. Hubbell,et al.  The unified neutral theory of biodiversity and biogeography at age ten. , 2011, Trends in ecology & evolution.

[19]  S. Pacala,et al.  Theory predicts a rapid transition from niche-structured to neutral biodiversity patterns across a speciation-rate gradient , 2011, Theoretical Ecology.

[20]  S. Langenheder,et al.  Species sorting and neutral processes are both important during the initial assembly of bacterial communities , 2011, The ISME Journal.

[21]  Michel Loreau,et al.  A mathematical synthesis of niche and neutral theories in community ecology. , 2011, Journal of theoretical biology.

[22]  L. Erijman,et al.  Balance of Neutral and Deterministic Components in the Dynamics of Activated Sludge Floc Assembly , 2011, Microbial Ecology.

[23]  Courtney J. Robinson,et al.  From Structure to Function: the Ecology of Host-Associated Microbial Communities , 2010, Microbiology and Molecular Biology Reviews.

[24]  Irina Dana Ofiteru,et al.  Combined niche and neutral effects in a microbial wastewater treatment community , 2010, Proceedings of the National Academy of Sciences.

[25]  Mark Vellend,et al.  Conceptual Synthesis in Community Ecology , 2010, The Quarterly Review of Biology.

[26]  Calvin Dytham,et al.  Relative roles of niche and neutral processes in structuring a soil microbial community , 2010, The ISME Journal.

[27]  A. Buckling,et al.  Quantifying the relative importance of niches and neutrality for coexistence in a model microbial system , 2009 .

[28]  Les Dethlefsen,et al.  The Pervasive Effects of an Antibiotic on the Human Gut Microbiota, as Revealed by Deep 16S rRNA Sequencing , 2008, PLoS biology.

[29]  N. Ostle,et al.  Microbial contributions to climate change through carbon cycle feedbacks , 2008, The ISME Journal.

[30]  W. Sloan,et al.  Neutral assembly of bacterial communities. , 2007, FEMS microbiology ecology.

[31]  D. Relman,et al.  An ecological and evolutionary perspective on human–microbe mutualism and disease , 2007, Nature.

[32]  Gerard Muyzer,et al.  A comparison of taxon co-occurrence patterns for macro- and microorganisms. , 2007, Ecology.

[33]  M. Kuypers,et al.  New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation , 2007, The ISME Journal.

[34]  Laura E. Green,et al.  The role of ecological theory in microbial ecology , 2007, Nature Reviews Microbiology.

[35]  Sallie W. Chisholm,et al.  Emergent Biogeography of Microbial Communities in a Model Ocean , 2007, Science.

[36]  T. Fukami,et al.  Immigration history controls diversification in experimental adaptive radiation , 2007, Nature.

[37]  Wenying Shou,et al.  Synthetic cooperation in engineered yeast populations , 2007, Proceedings of the National Academy of Sciences.

[38]  Peter B Adler,et al.  A niche for neutrality. , 2007, Ecology letters.

[39]  Tom Curtis,et al.  Influence of Sustainability and Immigration in Assembling Bacterial Populations of Known Size and Function , 2007, Microbial Ecology.

[40]  S. Nee,et al.  Quantifying the roles of immigration and chance in shaping prokaryote community structure. , 2006, Environmental microbiology.

[41]  Dominique Gravel,et al.  Reconciling niche and neutrality: the continuum hypothesis. , 2006, Ecology letters.

[42]  R. Kassen,et al.  Distribution of fitness effects among beneficial mutations before selection in experimental populations of bacteria , 2006, Nature Genetics.

[43]  D. Relman,et al.  Methanogenic Archaea and human periodontal disease. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Michael Wagner,et al.  Microbial community composition and function in wastewater treatment plants , 2002, Antonie van Leeuwenhoek.

[45]  Graham H Fleet,et al.  The microbial ecology of cocoa bean fermentations in Indonesia. , 2003, International journal of food microbiology.

[46]  H. A. Orr,et al.  The distribution of fitness effects among beneficial mutations. , 2003, Genetics.

[47]  Michael D. Collins,et al.  The unified neutral theory of biodiversity and biogeography , 2002 .

[48]  S. Levin,et al.  Comparing Classical Community Models: Theoretical Consequences for Patterns of Diversity , 2002, The American Naturalist.

[49]  M Imhof,et al.  Fitness effects of advantageous mutations in evolving Escherichia coli populations. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Graham Bell,et al.  The Distribution of Abundance in Neutral Communities , 2000, The American Naturalist.

[51]  Daniel E Rozen,et al.  Long‐Term Experimental Evolution in Escherichia coli. VIII. Dynamics of a Balanced Polymorphism , 2000, The American Naturalist.

[52]  Ronald W. Davis,et al.  Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. , 1999, Science.

[53]  Potts,et al.  Can high tree species richness be explained by Hubbell’s null model? , 1998 .

[54]  Michael Travisano,et al.  Adaptive radiation in a heterogeneous environment , 1998, Nature.

[55]  Kui Lin,et al.  THE EFFECTS OF COMPETITIVE ASYMMETRY ON THE RATE OF COMPETITIVE DISPLACEMENT : HOW ROBUST IS HUBBELL'S COMMUNITY DRIFT MODEL? , 1997 .

[56]  J. Adams,et al.  Evolution of Escherichia coli during growth in a constant environment. , 1987, Genetics.

[57]  A. Shmida,et al.  Biological determinants of species diversity , 1985 .

[58]  Stephen P. Hubbell,et al.  Tree Dispersion, Abundance, and Diversity in a Tropical Dry Forest , 1979, Science.

[59]  J. Connell Diversity in tropical rain forests and coral reefs. , 1978, Science.

[60]  J. Lubchenco Plant Species Diversity in a Marine Intertidal Community: Importance of Herbivore Food Preference and Algal Competitive Abilities , 1978, The American Naturalist.

[61]  James H. Brown,et al.  Turnover Rates in Insular Biogeography: Effect of Immigration on Extinction , 1977 .

[62]  R. Macarthur,et al.  The Theory of Island Biogeography , 1969 .

[63]  F. W. Preston The Canonical Distribution of Commonness and Rarity: Part I , 1962 .

[64]  K. Atwood,et al.  Selective mechanisms in bacteria. , 1951, Cold Spring Harbor symposia on quantitative biology.

[65]  Rory A. Fisher,et al.  XVII—The distribution of gene ratios for rare mutations , 1931 .

[66]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[67]  A. J. Lotka Elements of Physical Biology. , 1925, Nature.