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      Conditionally Rare Taxa Disproportionately Contribute to Temporal Changes in Microbial Diversity

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          ABSTRACT

          Microbial communities typically contain many rare taxa that make up the majority of the observed membership, yet the contribution of this microbial “rare biosphere” to community dynamics is unclear. Using 16S rRNA amplicon sequencing of 3,237 samples from 42 time series of microbial communities from nine different ecosystems (air; marine; lake; stream; adult human skin, tongue, and gut; infant gut; and brewery wastewater treatment), we introduce a new method to detect typically rare microbial taxa that occasionally become very abundant (conditionally rare taxa [CRT]) and then quantify their contributions to temporal shifts in community structure. We discovered that CRT made up 1.5 to 28% of the community membership, represented a broad diversity of bacterial and archaeal lineages, and explained large amounts of temporal community dissimilarity (i.e., up to 97% of Bray-Curtis dissimilarity). Most of the CRT were detected at multiple time points, though we also identified “one-hit wonder” CRT that were observed at only one time point. Using a case study from a temperate lake, we gained additional insights into the ecology of CRT by comparing routine community time series to large disturbance events. Our results reveal that many rare taxa contribute a greater amount to microbial community dynamics than is apparent from their low proportional abundances. This observation was true across a wide range of ecosystems, indicating that these rare taxa are essential for understanding community changes over time.

          IMPORTANCE

          Microbial communities and their processes are the foundations of ecosystems. The ecological roles of rare microorganisms are largely unknown, but it is thought that they contribute to community stability by acting as a reservoir that can rapidly respond to environmental changes. We investigated the occurrence of typically rare taxa that very occasionally become more prominent in their communities (“conditionally rare”). We quantified conditionally rare taxa in time series from a wide variety of ecosystems and discovered that not only were conditionally rare taxa present in all of the examples, but they also contributed disproportionately to temporal changes in diversity when they were most abundant. This result indicates an important and general role for rare microbial taxa within their communities.

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          Most cited references 51

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          QIIME allows analysis of high-throughput community sequencing data.

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            An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea

            Reference phylogenies are crucial for providing a taxonomic framework for interpretation of marker gene and metagenomic surveys, which continue to reveal novel species at a remarkable rate. Greengenes is a dedicated full-length 16S rRNA gene database that provides users with a curated taxonomy based on de novo tree inference. We developed a ‘taxonomy to tree' approach for transferring group names from an existing taxonomy to a tree topology, and used it to apply the Greengenes, National Center for Biotechnology Information (NCBI) and cyanoDB (Cyanobacteria only) taxonomies to a de novo tree comprising 408 315 sequences. We also incorporated explicit rank information provided by the NCBI taxonomy to group names (by prefixing rank designations) for better user orientation and classification consistency. The resulting merged taxonomy improved the classification of 75% of the sequences by one or more ranks relative to the original NCBI taxonomy with the most pronounced improvements occurring in under-classified environmental sequences. We also assessed candidate phyla (divisions) currently defined by NCBI and present recommendations for consolidation of 34 redundantly named groups. All intermediate results from the pipeline, which includes tree inference, jackknifing and transfer of a donor taxonomy to a recipient tree (tax2tree) are available for download. The improved Greengenes taxonomy should provide important infrastructure for a wide range of megasequencing projects studying ecosystems on scales ranging from our own bodies (the Human Microbiome Project) to the entire planet (the Earth Microbiome Project). The implementation of the software can be obtained from http://sourceforge.net/projects/tax2tree/.
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              Microbial diversity in the deep sea and the underexplored "rare biosphere".

              The evolution of marine microbes over billions of years predicts that the composition of microbial communities should be much greater than the published estimates of a few thousand distinct kinds of microbes per liter of seawater. By adopting a massively parallel tag sequencing strategy, we show that bacterial communities of deep water masses of the North Atlantic and diffuse flow hydrothermal vents are one to two orders of magnitude more complex than previously reported for any microbial environment. A relatively small number of different populations dominate all samples, but thousands of low-abundance populations account for most of the observed phylogenetic diversity. This "rare biosphere" is very ancient and may represent a nearly inexhaustible source of genomic innovation. Members of the rare biosphere are highly divergent from each other and, at different times in earth's history, may have had a profound impact on shaping planetary processes.
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                Author and article information

                Affiliations
                [ a ]Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
                [ b ]Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana, USA
                [ c ]Institute for Genomic and Systems Biology, Argonne National Laboratory, Argonne, Illinois, USA
                [ d ]Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA
                [ e ]Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, USA
                [ f ]Howard Hughes Medical Institute, Boulder, Colorado, USA
                [ g ]Department of Chemistry and Biochemistry and BioFrontiers Institute, University of Colorado, Boulder, Colorado, USA
                [ h ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA
                [ i ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA
                [ j ]Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA
                Author notes
                Address correspondence to Jack A. Gilbert, gilbertjack@ 123456anl.gov .

                Editor Nicole Dubilier, Max Planck Institute for Marine Microbiology

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society of Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                15 July 2014
                Jul-Aug 2014
                : 5
                : 4
                25028427 4161262 mBio01371-14 10.1128/mBio.01371-14
                Copyright © 2014 Shade et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Counts
                Pages: 9
                Categories
                Research Article
                Custom metadata
                July/August 2014

                Life sciences

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