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      Neutrality in the Metaorganism

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          Abstract

          Almost all animals and plants are inhabited by diverse communities of microorganisms, the microbiota, thereby forming an integrated entity, the metaorganism. Natural selection should favor hosts that shape the community composition of these microbes to promote a beneficial host-microbe symbiosis. Indeed, animal hosts often pose selective environments, which only a subset of the environmentally available microbes are able to colonize. How these microbes assemble after colonization to form the complex microbiota is less clear. Neutral models are based on the assumption that the alternatives in microbiota community composition are selectively equivalent and thus entirely shaped by random population dynamics and dispersal. Here, we use the neutral model as a null hypothesis to assess microbiata composition in host organisms, which does not rely on invoking any adaptive processes underlying microbial community assembly. We show that the overall microbiota community structure from a wide range of host organisms, in particular including previously understudied invertebrates, is in many cases consistent with neutral expectations. Our approach allows to identify individual microbes that are deviating from the neutral expectation and are therefore interesting candidates for further study. Moreover, using simulated communities, we demonstrate that transient community states may play a role in the deviations from the neutral expectation. Our findings highlight that the consideration of neutral processes and temporal changes in community composition are critical for an in-depth understanding of microbiota-host interactions.

          Abstract

          A study of microbiome compositions from many animal host species across the tree of life reveals them to be consistent with neutral expectations, suggesting that after colonization, neutral processes and dispersal play a role in shaping host-associated microbial communities.

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          The microbiome and innate immunity.

          The intestinal microbiome is a signalling hub that integrates environmental inputs, such as diet, with genetic and immune signals to affect the host's metabolism, immunity and response to infection. The haematopoietic and non-haematopoietic cells of the innate immune system are located strategically at the host-microbiome interface. These cells have the ability to sense microorganisms or their metabolic products and to translate the signals into host physiological responses and the regulation of microbial ecology. Aberrations in the communication between the innate immune system and the gut microbiota might contribute to complex diseases.
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            Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.

            Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages--which provide a larger spatiotemporal scale relative to within stage analyses--revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended--and experimentally testable--conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems.
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              Relative roles of niche and neutral processes in structuring a soil microbial community.

              Most attempts to identify the processes that structure natural communities have focused on conspicuous macroorganisms whereas the processes responsible for structuring microbial communities remain relatively unknown. Two main theories explaining these processes have emerged; niche theory, which highlights the importance of deterministic processes, and neutral theory, which focuses on stochastic processes. We examined whether neutral or niche-based mechanisms best explain the composition and structure of communities of a functionally important soil microbe, the arbuscular mycorrhizal (AM) fungi. Using molecular techniques, we surveyed AM fungi from 425 individual plants of 28 plant species along a soil pH gradient. There was evidence that both niche and neutral processes structured this community. Species abundances fitted the zero-sum multinomial distribution and there was evidence of dispersal limitation, both indicators of neutral processes. However, we found stronger support that niche differentiation based on abiotic soil factors, primarily pH, was structuring the AM fungal community. Host plant species affected AM fungal community composition negligibly compared to soil pH. We conclude that although niche partitioning was the primary mechanism regulating the composition and diversity of natural AM fungal communities, these communities are also influenced by stochastic-neutral processes. This study represents one of the most comprehensive investigations of community-level processes acting on soil microbes; revealing a community that although influenced by stochastic processes, still responded in a predictable manner to a major abiotic niche axis, soil pH. The strong response to environmental factors of this community highlights the susceptibility of soil microbes to environmental change.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                19 June 2019
                June 2019
                19 June 2019
                : 17
                : 6
                : e3000298
                Affiliations
                [1 ] Max Planck Institute for Evolutionary Biology, Plön, Germany
                [2 ] GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany
                [3 ] Institute for General Microbiology, University of Kiel, Kiel, Germany
                [4 ] Zoological Institute, University of Kiel, Kiel, Germany
                [5 ] Institute of Microbiology, Chinese Academy of Science, Beijing, China
                [6 ] Institute for Clinical Molecular Biology, University of Kiel, Kiel, Germany
                [7 ] Institute for Experimental Medicine, University of Kiel, Kiel, Germany
                MIT, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2703-3665
                http://orcid.org/0000-0001-8284-1222
                http://orcid.org/0000-0003-0563-8970
                http://orcid.org/0000-0001-6374-4910
                http://orcid.org/0000-0002-0669-5267
                Article
                PBIOLOGY-D-18-00420
                10.1371/journal.pbio.3000298
                6583948
                31216282
                99eeb07a-7b13-45cf-be13-675fd3408266
                © 2019 Sieber 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 August 2018
                : 15 May 2019
                Page count
                Figures: 5, Tables: 0, Pages: 21
                Funding
                This research was supported by the Collaborative Research Centre 1182, "Origin and Function of Metaorganisms," funded by the Deutsche Forschungsgemeinschaft ( https://www.dfg.de). TCGB gratefully appreciates support from the Canadian Institute for Advanced Research. 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
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Ecology
                Community Ecology
                Community Structure
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Community Structure
                Biology and Life Sciences
                Taxonomy
                Microbial Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Microbial Taxonomy
                Biology and Life Sciences
                Ecology
                Community Ecology
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Caenorhabditis Elegans
                Research and Analysis Methods
                Model Organisms
                Caenorhabditis Elegans
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Animal Models
                Caenorhabditis Elegans
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Caenorhabditis
                Caenorhabditis Elegans
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Sponges
                Biology and Life Sciences
                Evolutionary Biology
                Population Genetics
                Neutral Theory
                Biology and Life Sciences
                Genetics
                Population Genetics
                Neutral Theory
                Biology and Life Sciences
                Population Biology
                Population Genetics
                Neutral Theory
                Biology and Life Sciences
                Population Biology
                Population Dynamics
                Custom metadata
                All relevant data are within the paper and its Supporting Information files ( S1S10 Data). Source code is available at https://github.com/misieber/neufit.

                Life sciences
                Life sciences

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