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      Available energy fluxes drive a transition in the diversity, stability, and functional structure of microbial communities

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          Abstract

          A fundamental goal of microbial ecology is to understand what determines the diversity, stability, and structure of microbial ecosystems. The microbial context poses special conceptual challenges because of the strong mutual influences between the microbes and their chemical environment through the consumption and production of metabolites. By analyzing a generalized consumer resource model that explicitly includes cross-feeding, stochastic colonization, and thermodynamics, we show that complex microbial communities generically exhibit a transition as a function of available energy fluxes from a “resource-limited” regime where community structure and stability is shaped by energetic and metabolic considerations to a diverse regime where the dominant force shaping microbial communities is the overlap between species’ consumption preferences. These two regimes have distinct species abundance patterns, different functional profiles, and respond differently to environmental perturbations. Our model reproduces large-scale ecological patterns observed across multiple experimental settings such as nestedness and differential beta diversity patterns along energy gradients. We discuss the experimental implications of our results and possible connections with disorder-induced phase transitions in statistical physics.

          Author summary

          The diversity, stability and functional structure of microbial communities have dramatic effects on the health of humans and of ecosystems. The complexity of these communities has so far precluded the development of a general predictive model that would capture the dependence of these features on environmental conditions. We confronted this challenge by constructing a flexible simulation framework, and randomly sampling parameters under a variety of modeling assumptions to identify generic patterns. We found two qualitatively distinct regimes of community structure, which reproduce observed patterns of biodiversity, and make new predictions about stability and function.

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          Most cited references33

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          Characteristic Vectors of Bordered Matrices With Infinite Dimensions

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            Community assembly: when should history matter?

            Community assembly provides a conceptual foundation for understanding the processes that determine which and how many species live in a particular locality. Evidence suggests that community assembly often leads to a single stable equilibrium, such that the conditions of the environment and interspecific interactions determine which species will exist there. In such cases, regions of local communities with similar environmental conditions should have similar community composition. Other evidence suggests that community assembly can lead to multiple stable equilibria. Thus, the resulting community depends on the assembly history, even when all species have access to the community. In these cases, a region of local communities with similar environmental conditions can be very dissimilar in their community composition. Both regional and local factors should determine the patterns by which communities assemble, and the resultant degree of similarity or dissimilarity among localities with similar environments. A single equilibrium in more likely to be realized in systems with small regional species pools, high rates of connectance, low productivity and high disturbance. Multiple stable equilibria are more likely in systems with large regional species pools, low rates of connectance, high productivity and low disturbance. I illustrate preliminary evidence for these predictions from an observational study of small pond communities, and show important effects on community similarity, as well as on local and regional species richness.
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              Emergent simplicity in microbial community assembly

              A major unresolved question in microbiome research is whether the complex taxonomic architectures observed in surveys of natural communities can be explained and predicted by fundamental, quantitative principles. Bridging theory and experiment is hampered by the multiplicity of ecological processes that simultaneously affect community assembly in natural ecosystems. We addressed this challenge by monitoring the assembly of hundreds of soil- and plant-derived microbiomes in well-controlled minimal synthetic media. Both the community-level function and the coarse-grained taxonomy of the resulting communities are highly predictable and governed by nutrient availability, despite substantial species variability. By generalizing classical ecological models to include widespread nonspecific cross-feeding, we show that these features are all emergent properties of the assembly of large microbial communities, explaining their ubiquity in natural microbiomes.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                February 2019
                5 February 2019
                : 15
                : 2
                : e1006793
                Affiliations
                [1 ] Department of Physics, Boston University, Boston, MA, USA
                [2 ] Department of Physics, Boston College, Chestnut Hill, MA, USA
                [3 ] Bioinformatics Program, Boston University, Boston, MA, USA
                [4 ] Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, USA
                Rutgers University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-5007-6877
                http://orcid.org/0000-0002-9900-5092
                http://orcid.org/0000-0001-7315-8018
                http://orcid.org/0000-0002-2292-5608
                Article
                PCOMPBIOL-D-18-01910
                10.1371/journal.pcbi.1006793
                6386421
                30721227
                e87cb48f-f8cf-4ec6-8cb2-aac94cbfb4d4
                © 2019 Marsland et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 9 November 2018
                : 15 January 2019
                Page count
                Figures: 7, Tables: 0, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100001309, Research Corporation for Science Advancement;
                Award ID: Scialog Program
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: 1R35GM119461
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100001309, Research Corporation for Science Advancement;
                Award ID: Cottrell Scholar Award
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: Simons Investigator in the Mathematical Modeling of Living Systems
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: Simons Investigator in the Mathematical Modeling of Living Systems
                Award Recipient :
                The funding for this work partly results from a Scialog Program sponsored jointly by Research Corporation for Science Advancement (RCSA) and the Gordon and Betty Moore Foundation ( http://rescorp.org/scialog). This work was also supported by NIH NIGMS grant 1R35GM119461 ( https://www.nigms.nih.gov/), by a Cottrell Scholar award from RCSA to KK ( http://rescorp.org/cottrell-scholars), and by Simons Investigator in the Mathematical Modeling of Living Systems (MMLS) awards to PM and KK ( https://www.simonsfoundation.org/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Community Ecology
                Community Structure
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Community Structure
                Biology and Life Sciences
                Ecology
                Biodiversity
                Ecology and Environmental Sciences
                Ecology
                Biodiversity
                Biology and Life Sciences
                Biochemistry
                Bioenergetics
                Biology and Life Sciences
                Ecology
                Community Ecology
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Biology and Life Sciences
                Ecology
                Ecosystems
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Biology and Life Sciences
                Ecology
                Microbial Ecology
                Ecology and Environmental Sciences
                Ecology
                Microbial Ecology
                Biology and Life Sciences
                Microbiology
                Microbial Ecology
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Biology and Life Sciences
                Ecology
                Community Ecology
                Community Assembly
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Community Assembly
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-02-22
                Simulation data files may be found at https://github.com/Emergent-Behaviors-in-Biology/crossfeeding-transition. Simulation code can be downloaded from https://github.com/Emergent-Behaviors-in-Biology/community-simulator.

                Quantitative & Systems biology
                Quantitative & Systems biology

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