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      Vertebrate Hosts as Islands: Dynamics of Selection, Immigration, Loss, Persistence, and Potential Function of Bacteria on Salamander Skin

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          Abstract

          Skin bacterial communities can protect amphibians from a fungal pathogen; however, little is known about how these communities are maintained. We used a neutral model of community ecology to identify bacteria that are maintained on salamanders by selection or by dispersal from a bacterial reservoir (soil) and ecological drift. We found that 75% (9/12) of bacteria that were consistent with positive selection, <1% of bacteria that were consistent with random dispersal and none of the bacteria that were consistent under negative selection had a 97% or greater match to antifungal isolates. Additionally we performed an experiment where salamanders were either provided or denied a bacterial reservoir and estimated immigration and loss (emigration and local extinction) rates of bacteria on salamanders in both treatments. Loss was strongly related to bacterial richness, suggesting competition is important for structuring the community. Bacteria closely related to antifungal isolates were more likely to persist on salamanders with or without a bacterial reservoir, suggesting they had a competitive advantage. Furthermore, over-represented and under-represented operational taxonomic units (OTUs) had similar persistence on salamanders when a bacterial reservoir was present. However, under-represented OTUs were less likely to persist in the absence of a bacterial reservoir, suggesting that the over-represented and under-represented bacteria were selected against or for on salamanders through time. Our findings from the neutral model, migration and persistence analyses show that bacteria that exhibit a high similarity to antifungal isolates persist on salamanders, which likely protect hosts against pathogens and improve fitness. This research is one of the first to apply ecological theory to investigate assembly of host associated-bacterial communities, which can provide insights for probiotic bioaugmentation as a conservation strategy against disease.

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            Patterns and processes of microbial community assembly.

            Recent research has expanded our understanding of microbial community assembly. However, the field of community ecology is inaccessible to many microbial ecologists because of inconsistent and often confusing terminology as well as unnecessarily polarizing debates. Thus, we review recent literature on microbial community assembly, using the framework of Vellend (Q. Rev. Biol. 85:183-206, 2010) in an effort to synthesize and unify these contributions. We begin by discussing patterns in microbial biogeography and then describe four basic processes (diversification, dispersal, selection, and drift) that contribute to community assembly. We also discuss different combinations of these processes and where and when they may be most important for shaping microbial communities. The spatial and temporal scales of microbial community assembly are also discussed in relation to assembly processes. Throughout this review paper, we highlight differences between microbes and macroorganisms and generate hypotheses describing how these differences may be important for community assembly. We end by discussing the implications of microbial assembly processes for ecosystem function and biodiversity.
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              Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

              Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                16 March 2016
                2016
                : 7
                : 333
                Affiliations
                [1] 1Department of Biology, James Madison University, Harrisonburg VA, USA
                [2] 2Department of Internal Medicine, University of Michigan, Ann Arbor MI, USA
                [3] 3BioFrontiers Institute, University of Colorado, Boulder CO, USA
                [4] 4Department of Ecology and Evolutionary Biology, University of Colorado, Boulder CO, USA
                Author notes

                Edited by: Thomas Carl Bosch, Kiel University, Germany

                Reviewed by: Sebastian Fraune, Christian-Albrechts-Universitãt Kiel, Germany; Mark J. Mandel, Northwestern University Feinberg School of Medicine, USA

                *Correspondence: Andrew H. Loudon, loudon@ 123456zoology.ubc.ca

                Present address: Andrew H. Loudon, Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada; William Van Treuren, Department of Microbiology and Immunology, Stanford University, Stanford, CA, USA; Douglas C. Woodhams, Department of Biology, University of Massachusetts Boston, Boston, MA, USA; Laura Wegener Parfrey, Department of Zoology and Biodiversity Research Centre, and Department of Botany, University of British Columbia, Vancouver, BC, Canada; Rob Knight, Howard Hughes Medical Institute, University of Colorado, Boulder, CO, USA; School of Medicine, University of California San Diego, La Jolla, CA, USA

                This article was submitted to Microbial Symbioses, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2016.00333
                4793798
                27014249
                4a0e5966-885a-4eb9-afa7-5eec236236f4
                Copyright © 2016 Loudon, Venkataraman, Van Treuren, Woodhams, Parfrey, McKenzie, Knight, Schmidt and Harris.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 January 2016
                : 02 March 2016
                Page count
                Figures: 3, Tables: 2, Equations: 0, References: 54, Pages: 11, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: DEB 1136602
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: DEB 1146284
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: T32 HL007749
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                neutral model,host-associated microbial communities,island biogeography,plethodon cinereus,batrachochytrium dendrobatidis,symbiosis,antifungal

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