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      A communal catalogue reveals Earth’s multiscale microbial diversity

      research-article
      1 , 2 , 3 , 1 , 1 , 1 , 4 , 5 , 6 , 1 , 7 , 8 , 9 , 10 , 1 , 1 , 11 , 1 , 1 , 1 , 11 , 1 , 1 , 11 , 12 , 1 , 1 , 13 , 14 , 1 , 1 , 1 , 1 , 15 , 1 , 16 , 1 , 17 , 17 , 18 , 19 , 20 , 20 , 21 , 22 , 19 , 23 , 24 , 25 , 26 , 27 , 28 , 4 , 3 , 16 , , 17 , 29 , , 1 , 11 , 30 , , The Earth Microbiome Project Consortium
      Nature
      Nature Publishing Group UK
      Environmental microbiology, Microbiome

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          Abstract

          Our growing awareness of the microbial world’s importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth’s microbial diversity.

          Supplementary information

          The online version of this article (doi:10.1038/nature24621) contains supplementary material, which is available to authorized users.

          Abstract

          As phase 1 of the Earth Microbiome Project, analysis of 16S ribosomal RNA sequences from more than 27,000 environmental samples delivers a global picture of the basic structure and drivers of microbial distribution.

          Supplementary information

          The online version of this article (doi:10.1038/nature24621) contains supplementary material, which is available to authorized users.

          Earth's microbial diversity

          In this meta-analysis of studies from the Earth Microbiome Project, Luke Thompson et al. have developed a standardized collection, curation and analysis pipeline to examine 16S ribosomal RNA (rRNA) tag sequences of more than 27,000 samples (representing soil, water, animal-associated and plant-associated habitats), providing global context for the basic structure and drivers of bacterial and archaeal distribution. The work not only provides an important reference database and framework for future studies in microbial ecology, but also reveals patterns in community composition as well as the global distribution of particular organisms. These findings provide a deeper understanding of dispersal and niche colonization.

          Supplementary information

          The online version of this article (doi:10.1038/nature24621) contains supplementary material, which is available to authorized users.

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          Most cited references35

          • Record: found
          • Abstract: found
          • Article: found
          Is Open Access

          EMPeror: a tool for visualizing high-throughput microbial community data

          Background As microbial ecologists take advantage of high-throughput sequencing technologies to describe microbial communities across ever-increasing numbers of samples, new analysis tools are required to relate the distribution of microbes among larger numbers of communities, and to use increasingly rich and standards-compliant metadata to understand the biological factors driving these relationships. In particular, the Earth Microbiome Project drives these needs by profiling the genomic content of tens of thousands of samples across multiple environment types. Findings Features of EMPeror include: ability to visualize gradients and categorical data, visualize different principal coordinates axes, present the data in the form of parallel coordinates, show taxa as well as environmental samples, dynamically adjust the size and transparency of the spheres representing the communities on a per-category basis, dynamically scale the axes according to the fraction of variance each explains, show, hide or recolor points according to arbitrary metadata including that compliant with the MIxS family of standards developed by the Genomic Standards Consortium, display jackknifed-resampled data to assess statistical confidence in clustering, perform coordinate comparisons (useful for procrustes analysis plots), and greatly reduce loading times and overall memory footprint compared with existing approaches. Additionally, ease of sharing, given EMPeror’s small output file size, enables agile collaboration by allowing users to embed these visualizations via emails or web pages without the need for extra plugins. Conclusions Here we present EMPeror, an open source and web browser enabled tool with a versatile command line interface that allows researchers to perform rapid exploratory investigations of 3D visualizations of microbial community data, such as the widely used principal coordinates plots. EMPeror includes a rich set of controllers to modify features as a function of the metadata. By being specifically tailored to the requirements of microbial ecologists, EMPeror thus increases the speed with which insight can be gained from large microbiome datasets.
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            A new generation of homology search tools based on probabilistic inference.

            Many theoretical advances have been made in applying probabilistic inference methods to improve the power of sequence homology searches, yet the BLAST suite of programs is still the workhorse for most of the field. The main reason for this is practical: BLAST's programs are about 100-fold faster than the fastest competing implementations of probabilistic inference methods. I describe recent work on the HMMER software suite for protein sequence analysis, which implements probabilistic inference using profile hidden Markov models. Our aim in HMMER3 is to achieve BLAST's speed while further improving the power of probabilistic inference based methods. HMMER3 implements a new probabilistic model of local sequence alignment and a new heuristic acceleration algorithm. Combined with efficient vector-parallel implementations on modern processors, these improvements synergize. HMMER3 uses more powerful log-odds likelihood scores (scores summed over alignment uncertainty, rather than scoring a single optimal alignment); it calculates accurate expectation values (E-values) for those scores without simulation using a generalization of Karlin/Altschul theory; it computes posterior distributions over the ensemble of possible alignments and returns posterior probabilities (confidences) in each aligned residue; and it does all this at an overall speed comparable to BLAST. The HMMER project aims to usher in a new generation of more powerful homology search tools based on probabilistic inference methods.
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              • Abstract: found
              • Article: not found

              Fast UniFrac: Facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data

              Next-generation sequencing techniques, and PhyloChip, have made simultaneous phylogenetic analyses of hundreds of microbial communities possible. Insight into community structure has been limited by the inability to integrate and visualize such vast datasets. Fast UniFrac overcomes these issues, allowing integration of larger numbers of sequences and samples into a single analysis. Its new array-based implementation offers orders of magnitude improvements over the original version. New 3D visualization of principal coordinates analysis (PCoA) results, with the option to view multiple coordinate axes simultaneously, provides a powerful way to quickly identify patterns that relate vast numbers of microbial communities. We demonstrate the potential of Fast UniFrac using examples from three data types: Sanger-sequencing studies of diverse free-living and animal-associated bacterial assemblages and from the gut of obese humans as they diet, pyrosequencing data integrated from studies of the human hand and gut, and PhyloChip data from a study of citrus pathogens. We show that a Fast UniFrac analysis using a reference tree recaptures patterns that could not be detected without considering phylogenetic relationships and that Fast UniFrac, coupled with BLAST-based sequence assignment, can be used to quickly analyze pyrosequencing runs containing hundreds of thousands of sequences, revealing patterns relating human and gut samples. Finally, we show that the application of Fast UniFrac to PhyloChip data could identify well-defined subcategories associated with infection. Together, these case studies point the way towards a broad range of applications and demonstrate some of the new features of Fast UniFrac.
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                Author and article information

                Contributors
                janet.jansson@pnnl.gov
                gilbertjack@gmail.com
                robknight@ucsd.edu
                Journal
                Nature
                Nature
                Nature
                Nature Publishing Group UK (London )
                0028-0836
                1476-4687
                1 November 2017
                1 November 2017
                2017
                : 551
                : 7681
                : 457-463
                Affiliations
                [1 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Department of Pediatrics, , University of California San Diego, ; La Jolla, California USA
                [2 ]GRID grid.267193.8, ISNI 0000 0001 2295 628X, Department of Biological Sciences and Northern Gulf Institute, , University of Southern Mississippi, ; Hattiesburg, Mississippi USA
                [3 ]GRID grid.473842.e, ISNI 0000 0004 0601 1528, Ocean Chemistry and Ecosystems Division, , Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, stationed at Southwest Fisheries Science Center, ; La Jolla, California USA
                [4 ]GRID grid.266102.1, ISNI 0000 0001 2297 6811, The Gladstone Institutes and University of California San Francisco, ; San Francisco, California USA
                [5 ]GRID grid.411377.7, ISNI 0000 0001 0790 959X, Department of Biology, , Indiana University, ; Bloomington, Indiana USA
                [6 ]GRID grid.481551.c, Industrial and Applied Genomics, IBM Almaden Research Center, ; San Jose, California USA
                [7 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Division of Biological Sciences, , University of California San Diego, ; La Jolla, California USA
                [8 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Skaggs School of Pharmacy, University of California San Diego, ; La Jolla, California USA
                [9 ]GRID grid.116068.8, ISNI 0000 0001 2341 2786, Department of Biological Engineering, , Massachusetts Institute of Technology, ; Cambridge, Massachusetts USA
                [10 ]GRID grid.66859.34, The Broad Institute of MIT and Harvard, ; Cambridge, Massachusetts USA
                [11 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Department of Computer Science and Engineering, , University of California San Diego, ; La Jolla, California USA
                [12 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Department of Electrical and Computer Engineering, , University of California San Diego, ; La Jolla, California USA
                [13 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Department of Family Medicine and Public Health, , University of California San Diego, ; La Jolla, California USA
                [14 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Organismic and Evolutionary Biology, , Harvard University, ; Cambridge, Massachusetts USA
                [15 ]GRID grid.261120.6, ISNI 0000 0004 1936 8040, Pathogen and Microbiome Institute, Northern Arizona University, ; Flagstaff, Arizona USA
                [16 ]GRID grid.451303.0, ISNI 0000 0001 2218 3491, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, ; Richland, Washington USA
                [17 ]GRID grid.187073.a, ISNI 0000 0001 1939 4845, Biosciences Division, , Argonne National Laboratory, ; Argonne, Illinois USA
                [18 ]GRID grid.185648.6, ISNI 0000 0001 2175 0319, Department of Biological Sciences, , University of Illinois at Chicago, ; Chicago, Illinois USA
                [19 ]GRID grid.266190.a, ISNI 0000000096214564, BioFrontiers Institute, University of Colorado, ; Boulder, Colorado USA
                [20 ]GRID grid.266190.a, ISNI 0000000096214564, Department of Ecology and Evolutionary Biology, , University of Colorado, ; Boulder, Colorado USA
                [21 ]GRID grid.464551.7, ISNI 0000 0004 0450 3000, Cooperative Institute for Research in Environmental Sciences, University of Colorado, ; Boulder, Colorado USA
                [22 ]GRID grid.42505.36, ISNI 0000 0001 2156 6853, Department of Biological Sciences, , University of Southern California, ; Los Angeles, California USA
                [23 ]GRID grid.266190.a, ISNI 0000000096214564, Department of Computer Science, , University of Colorado, ; Boulder, Colorado USA
                [24 ]GRID grid.187073.a, ISNI 0000 0001 1939 4845, Computing, Environment and Life Sciences, Argonne National Laboratory, ; Argonne, Illinois USA
                [25 ]GRID grid.170205.1, ISNI 0000 0004 1936 7822, Department of Computer Science, , University of Chicago, ; Chicago, Illinois USA
                [26 ]GRID grid.17088.36, ISNI 0000 0001 2150 1785, Department of Microbiology and Molecular Genetics, , Michigan State University, ; East Lansing, Michigan USA
                [27 ]GRID grid.17088.36, ISNI 0000 0001 2150 1785, Department of Plant, , Soil and Microbial Sciences, Michigan State University, ; East Lansing, Michigan USA
                [28 ]GRID grid.17088.36, ISNI 0000 0001 2150 1785, Program in Ecology, Evolutionary Biology and Behavior, Michigan State University, ; East Lansing, Michigan USA
                [29 ]GRID grid.170205.1, ISNI 0000 0004 1936 7822, Department of Surgery, , University of Chicago, ; Chicago, Illinois USA
                [30 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, Center for Microbiome Innovation, University of California San Diego, ; La Jolla, California USA
                [31 ]GRID grid.267033.3, ISNI 0000 0004 0462 1680, University of Puerto Rico, ; San Juan, Puerto Rico USA
                [32 ]GRID grid.22319.3b, ISNI 0000000121062153, Plymouth Marine Laboratory, ; Plymouth, England UK
                [33 ]GRID grid.170205.1, ISNI 0000 0004 1936 7822, University of Chicago, ; Chicago, Illinois USA
                [34 ]GRID grid.16753.36, ISNI 0000 0001 2299 3507, Northwestern University, ; Evanston, Illinois USA
                [35 ]GRID grid.260293.c, ISNI 0000 0001 2162 4400, Mount Holyoke College, ; South Hadley, Massachusetts USA
                [36 ]GRID grid.5386.8, ISNI 000000041936877X, Cornell University, Ithaca, ; New York, USA
                [37 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, University of Tübingen, ; Tübingen, Germany
                [38 ]GRID grid.187073.a, ISNI 0000 0001 1939 4845, Argonne National Laboratory, ; Argonne, Illinois USA
                [39 ]GRID grid.56466.37, ISNI 0000 0004 0504 7510, Woods Hole Oceanographic Institution, ; Woods Hole, Massachusetts USA
                [40 ]GRID grid.47840.3f, ISNI 0000 0001 2181 7878, University of California Berkeley, ; Berkeley, California USA
                [41 ]GRID grid.131063.6, ISNI 0000 0001 2168 0066, University of Notre Dame, ; South Bend, Indiana USA
                [42 ]GRID grid.14509.39, ISNI 0000 0001 2166 4904, University of South Bohemia, ; Cˇeské Bude˘jovice, Czech Republic
                [43 ]GRID grid.143640.4, ISNI 0000 0004 1936 9465, University of Victoria, ; Victoria, British Columbia Canada
                [44 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, University of California Davis, ; Davis, California USA
                [45 ]GRID grid.444300.7, ISNI 0000 0004 1802 3198, Maharshi Dayanand Saraswati University, ; Ajmer, India
                [46 ]GRID grid.33489.35, ISNI 0000 0001 0454 4791, University of Delaware, ; Newark, Delaware USA
                [47 ]GRID grid.462844.8, ISNI 0000 0001 2308 1657, Université Pierre et Marie Curie, Evolution Paris Seine, ; Paris, France
                [48 ]GRID grid.260731.1, ISNI 0000 0001 2324 0259, National University of Mongolia, ; Ulaanbaatar, Mongolia
                [49 ]GRID grid.451303.0, ISNI 0000 0001 2218 3491, Pacific Northwest National Laboratory, ; Richland, Washington USA
                [50 ]GRID grid.269823.4, ISNI 0000 0001 2164 6888, Wildlife Conservation Society and Bronx Zoo, ; New York, New York USA
                [51 ]GRID grid.452788.4, ISNI 0000 0004 0458 5309, San Diego Zoo Institute for Conservation Research, ; Escondido, California USA
                [52 ]GRID grid.223827.e, ISNI 0000 0001 2193 0096, University of Utah, ; Salt Lake City, Utah USA
                [53 ]GRID grid.25627.34, ISNI 0000 0001 0790 5329, Manchester Metropolitan University, ; Manchester, UK
                [54 ]GRID grid.1005.4, ISNI 0000 0004 4902 0432, University of New South Wales, ; Sydney, New South Wales Australia
                [55 ]GRID grid.261120.6, ISNI 0000 0004 1936 8040, Northern Arizona University, ; Flagstaff, Arizona USA
                [56 ]GRID grid.10919.30, ISNI 0000000122595234, UiT-The Arctic University of Norway, ; Tromsø, Norway
                [57 ]GRID grid.49481.30, ISNI 0000 0004 0408 3579, University of Waikato, ; Hamilton, New Zealand
                [58 ]GRID grid.25879.31, ISNI 0000 0004 1936 8972, University of Pennsylvania, ; Philadelphia, Pennsylvania USA
                [59 ]GRID grid.46078.3d, ISNI 0000 0000 8644 1405, University of Waterloo, ; Waterloo, Ontario Canada
                [60 ]GRID grid.458485.0, ISNI 0000 0001 2156 4508, Institute of Soil Science, Chinese Academy of Sciences, ; Nanjing, China
                [61 ]GRID grid.410334.1, ISNI 0000 0001 2184 7612, Environment and Climate Change Canada, ; Saskatoon, Canada
                [62 ]GRID grid.17635.36, ISNI 0000000419368657, University of Minnesota, ; Saint Paul, Minnesota USA
                [63 ]GreenViet Biodiversity Conservation Center, Da Nang, Viet Nam
                [64 ]GRID grid.59734.3c, ISNI 0000 0001 0670 2351, Icahn School of Medicine at Mount Sinai, ; New York, New York USA
                [65 ]GRID grid.47894.36, ISNI 0000 0004 1936 8083, Colorado State University, ; Fort Collins, Colorado USA
                [66 ]GRID grid.6142.1, ISNI 0000 0004 0488 0789, National University of Ireland, ; Galway, Ireland
                [67 ]GRID grid.164295.d, ISNI 0000 0001 0941 7177, University of Maryland, ; College Park, Maryland USA
                [68 ]GRID grid.418243.8, ISNI 0000 0001 2181 3287, Instituto Venezolano de Investigaciones Cientificas (IVIC), ; Venezuela
                [69 ]GRID grid.28803.31, ISNI 0000 0001 0701 8607, University of Wisconsin, ; Madison, Wisconsin USA
                [70 ]GRID grid.7362.0, ISNI 0000000118820937, Bangor University, ; Bangor, Gwynedd UK
                [71 ]GRID grid.264889.9, ISNI 0000 0001 1940 3051, College of William and Mary, ; Williamsburg, Virginia USA
                [72 ]GRID grid.4391.f, ISNI 0000 0001 2112 1969, Oregon State University, ; Corvallis, Oregon USA
                [73 ]Beijing Zoo, Beijing, China
                [74 ]GRID grid.169077.e, ISNI 0000 0004 1937 2197, Purdue University, ; West Lafayette, Indiana USA
                [75 ]GRID grid.36425.36, ISNI 0000 0001 2216 9681, Stony Brook University, ; Stony Brook, New York USA
                [76 ]GRID grid.266876.b, ISNI 0000 0001 2156 9982, University of Northern British Columbia, Prince George, ; British, Columbia Canada
                [77 ]GRID grid.121334.6, ISNI 0000 0001 2097 0141, Université de Montpellier, ; CNRS, Montpellier France
                [78 ]Centro para el Estudio de Sistemas Marinos (CESIMAR-CONICET), CCT CENPAT, Puerto Madryn, Chubut Argentina
                [79 ]GRID grid.137628.9, ISNI 0000 0004 1936 8753, New York University, ; New York, New York USA
                [80 ]GRID grid.266190.a, ISNI 0000000096214564, University of Colorado, ; Boulder, Colorado USA
                [81 ]GRID grid.184769.5, ISNI 0000 0001 2231 4551, Lawrence Berkeley National Laboratory, ; Berkeley, California USA
                [82 ]GRID grid.267468.9, ISNI 0000 0001 0695 7223, University of Wisconsin, ; Milwaukee, Wisconsin USA
                [83 ]GRID grid.4691.a, ISNI 0000 0001 0790 385X, University of Naples Federico II, ; Naples, Italy
                [84 ]GRID grid.253563.4, ISNI 0000 0001 0657 9381, California State University, ; Northridge, California USA
                [85 ]GRID grid.213876.9, ISNI 0000 0004 1936 738X, University of Georgia, ; Athens, Georgia USA
                [86 ]GRID grid.152326.1, ISNI 0000 0001 2264 7217, Vanderbilt University, ; Nashville, Tennessee USA
                [87 ]GRID grid.170430.1, ISNI 0000 0001 2159 2859, University of Central Florida, ; Orlando, Florida USA
                [88 ]GRID grid.448381.2, ISNI 0000 0004 0628 1499, Minnesota Department of Natural Resources, ; St. Paul, Minnesota USA
                [89 ]GRID grid.1008.9, ISNI 0000 0001 2179 088X, University of Melbourne, ; Melbourne, Victoria Australia
                [90 ]GRID grid.35155.37, ISNI 0000 0004 1790 4137, Huazhong Agricultural University, ; Wuhan, Hubei China
                [91 ]GRID grid.10894.34, ISNI 0000 0001 1033 7684, Alfred Wegener Institute, ; Bremerhaven, Germany
                [92 ]GRID grid.4367.6, ISNI 0000 0001 2355 7002, Washington University, ; St. Louis, Missouri USA
                [93 ]GRID grid.7048.b, ISNI 0000 0001 1956 2722, Aarhus University, ; Aarhus, Denmark
                [94 ]GRID grid.7914.b, ISNI 0000 0004 1936 7443, University of Bergen, ; Bergen, Norway
                [95 ]GRID grid.264889.9, ISNI 0000 0001 1940 3051, Virginia Institute of Marine Science, ; Gloucester Point, Virginia USA
                [96 ]GRID grid.419247.d, ISNI 0000 0001 2108 8097, Leibniz Institute for Freshwater Ecology and Inland Fisheries, ; Stechlin, Germany
                [97 ]GRID grid.11348.3f, ISNI 0000 0001 0942 1117, Potsdam University, ; Potsdam, Germany
                [98 ]GRID grid.214458.e, ISNI 0000000086837370, University of Michigan, ; Ann Arbor, Michigan USA
                [99 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, The Ohio State University College of Veterinary Medicine, ; Columbus, Ohio USA
                [100 ]GRID grid.17091.3e, ISNI 0000 0001 2288 9830, University of British Columbia, Vancouver, ; British, Columbia Canada
                [101 ]ECOSCOPE Training Program, Vancouver, British Columbia Canada
                [102 ]GRID grid.9654.e, ISNI 0000 0004 0372 3343, University of Auckland, ; Auckland, New Zealand
                [103 ]GRID grid.468069.5, ISNI 0000 0004 0407 4680, Melbourne Water Corporation, ; Melbourne, Victoria Australia
                [104 ]GRID grid.21729.3f, ISNI 0000000419368729, Columbia University, ; New York, New York USA
                [105 ]Amazonic Center for Research and Control of Tropical Diseases (CAICET), Puerto Ayacucho, Amazonas Venezuela
                [106 ]GRID grid.34421.30, ISNI 0000 0004 1936 7312, Iowa State University, ; Ames, Iowa USA
                [107 ]GRID grid.421136.3, ISNI 0000 0000 9227 6872, Chief Dull Knife College, ; Lame Deer, Montana USA
                [108 ]GRID grid.8761.8, ISNI 0000 0000 9919 9582, University of Gothenburg, ; Gothenburg, Sweden
                [109 ]GRID grid.7737.4, ISNI 0000 0004 0410 2071, University of Helsinki, ; Helsinki, Finland
                [110 ]GRID grid.266100.3, ISNI 0000 0001 2107 4242, University of California San Diego, ; La Jolla, California USA
                [111 ]GRID grid.4830.f, ISNI 0000 0004 0407 1981, University of Groningen, ; Groningen, The Netherlands
                [112 ]GRID grid.1042.7, The Walter and Eliza Hall Institute of Medical Research, ; Parkville, Victoria Australia
                [113 ]GRID grid.265122.0, ISNI 0000 0001 0719 7561, Towson University, ; Towson, Maryland USA
                [114 ]GRID grid.213917.f, ISNI 0000 0001 2097 4943, Georgia Institute of Technology, ; Atlanta, Georgia USA
                [115 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Wageningen University and Research, ; Wageningen, Netherlands
                [116 ]GRID grid.8536.8, ISNI 0000 0001 2294 473X, Universidade Federal do Rio de Janeiro, ; Rio de Janeiro, Brazil
                [117 ]Nanoxis Consulting AB, Gothenburg, Sweden
                [118 ]Bio-Path Holdings, Inc., Texas, Bellaire USA
                [119 ]GRID grid.430387.b, ISNI 0000 0004 1936 8796, Rutgers University, ; New Brunswick, New Jersey USA
                [120 ]GRID grid.64337.35, ISNI 0000 0001 0662 7451, Louisiana State University, ; Baton Rouge, Louisiana USA
                [121 ]GRID grid.438006.9, ISNI 0000 0001 2296 9689, Smithsonian Tropical Research Institute, ; Balboa, Ancon Panama
                [122 ]GRID grid.258264.f, ISNI 0000 0004 0412 9645, Juniata College, ; Huntingdon, Pennsylvania USA
                [123 ]GRID grid.431413.0, ISNI 0000 0000 9909 027X, Fontbonne University, ; St. Louis, Missouri USA
                [124 ]GRID grid.55602.34, ISNI 0000 0004 1936 8200, Dalhousie University, ; Halifax, Nova Scotia Canada
                [125 ]GRID grid.117476.2, ISNI 0000 0004 1936 7611, University of Technology, ; Sydney, New South Wales Australia
                [126 ]Colección Ornitologica W. H. Phelps, Caracas, Venezuela
                [127 ]GRID grid.424923.a, ISNI 0000 0001 2035 1455, Institute of Botany, Czech Academy of Sciences, ; Dukelská, Trebon Czech Republic
                [128 ]GRID grid.458475.f, ISNI 0000 0004 1799 2309, Institute of Applied Ecology, Chinese Academy of Sciences, ; Shenyang, China
                [129 ]GRID grid.263081.e, ISNI 0000 0001 0790 1491, San Diego State University, ; San Diego, California USA
                [130 ]GRID grid.458451.9, ISNI 0000 0004 0644 4980, Institute of Tibetan Plateau Research, Chinese Academy of Sciences, ; Beijing, China
                [131 ]GRID grid.7345.5, ISNI 0000 0001 0056 1981, Universidad de Buenos Aires, ; Ciudad Autónoma de, Buenos Aires Argentina
                [132 ]GRID grid.469960.4, ISNI 0000 0004 0445 9505, Instituto Antártico Argentino, ; Buenos Aires, Argentina
                [133 ]GRID grid.4489.1, ISNI 0000000121678994, University of Granada, ; Granada, Spain
                [134 ]GRID grid.255986.5, ISNI 0000 0004 0472 0419, Florida State University, ; Tallahassee, Florida USA
                [135 ]GRID grid.264784.b, ISNI 0000 0001 2186 7496, Texas Tech University, ; Lubbock, Texas USA
                [136 ]GRID grid.168010.e, ISNI 0000000419368956, Stanford University, ; Stanford, California USA
                [137 ]GRID grid.170202.6, ISNI 0000 0004 1936 8008, University of Oregon, ; Eugene, Oregon USA
                [138 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, Pennsylvania State University, ; State College, Pennsylvania USA
                [139 ]Zoo Atlanta, Atlanta, Georgia USA
                [140 ]GRID grid.20627.31, ISNI 0000 0001 0668 7841, Ohio University, ; Athens, Ohio USA
                [141 ]CREA - Centro Agricoltura e Ambiente (CREA-AA), Florence, Italy
                [142 ]GRID grid.429319.4, ISNI 0000 0004 0464 4436, Morningside College, ; Sioux City, Iowa USA
                [143 ]GRID grid.259956.4, ISNI 0000 0001 2195 6763, Miami University, ; Oxford, Ohio USA
                [144 ]GRID grid.25697.3f, ISNI 0000 0001 2172 4233, Université de Lyon, ; Lyon, France
                [145 ]GRID grid.452414.2, Fanjingshan National Nature Reserve Administration, ; Tongren, China
                [146 ]GRID grid.7605.4, ISNI 0000 0001 2336 6580, University of Turin, ; Turin, Italy
                [147 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Natural History Museum of Denmark, ; Copenhagen, Denmark
                [148 ]Université de Toulouse, Université Paul Sabatier, Toulouse, France
                [149 ]GRID grid.448684.2, ISNI 0000 0004 4909 3041, Elizade University, ; Ilara-Mokin, Ondo State Nigeria
                [150 ]GRID grid.418810.4, ISNI 0000 0001 0018 8275, Emerson College, ; Boston, Massachusetts USA
                [151 ]GRID grid.422756.0, ISNI 0000 0004 0412 7324, Novozymes North America Inc., ; Raleigh-Durham, North Carolina USA
                [152 ]GRID grid.252547.3, ISNI 0000 0001 0705 7067, Auckland University of Technology, ; Auckland, New Zealand
                [153 ]GRID grid.262273.0, ISNI 0000 0001 2188 3760, City University of New York, ; New York, New York USA
                [154 ]GRID grid.7372.1, ISNI 0000 0000 8809 1613, University of Warwick, ; Coventry, UK
                [155 ]GRID grid.185648.6, ISNI 0000 0001 2175 0319, University of Illinois, ; Chicago, Illinois USA
                [156 ]GRID grid.16890.36, ISNI 0000 0004 1764 6123, The Hong Kong Polytechnic University, ; Hong Kong, China
                [157 ]GEOMAR Helmholtz Center for Ocean Research Kiel, Kiel, Germany
                [158 ]GRID grid.8273.e, ISNI 0000 0001 1092 7967, University of East Anglia, ; Norwich, UK
                [159 ]Department of Environmental Protection and Natural Resources, Northern Cheyenne Tribe, Lame Deer, Montana USA
                [160 ]GRID grid.17088.36, ISNI 0000 0001 2150 1785, Michigan State University, ; East Lansing, Michigan USA
                [161 ]Hybla Valley Veterinary Hospital, Alexandria, Virginia USA
                [162 ]Biota Technology Inc., San Diego, California USA
                [163 ]GRID grid.21106.34, ISNI 0000000121820794, University of Maine, ; Orono, Maine USA
                [164 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, University of Copenhagen, ; Copenhagen, Denmark
                [165 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Emory University, ; Atlanta, Georgia USA
                [166 ]GRID grid.263333.4, ISNI 0000 0001 0727 6358, Sejong University, ; Seoul, South Korea
                [167 ]GRID grid.411959.1, ISNI 0000 0004 1936 9633, Acadia University, ; Wolfville, Nova Scotia Canada
                [168 ]GRID grid.17063.33, ISNI 0000 0001 2157 2938, University of Toronto, ; Toronto, Ontario Canada
                [169 ]Independent Ornithologist, Merced, California USA
                [170 ]GRID grid.412654.0, ISNI 0000 0001 0679 2457, Södertörn University, ; Huddinge, Sweden
                [171 ]GRID grid.39382.33, ISNI 0000 0001 2160 926X, Baylor College of Medicine, ; Houston, Texas USA
                [172 ]GRID grid.466639.8, ISNI 0000 0004 0547 1725, Estación Experimental de Zonas Áridas (EEZA-CSIC), ; Almería, Spain
                [173 ]GRID grid.62813.3e, ISNI 0000 0004 1936 7806, Illinois Institute of Technology, ; Chicago, Illinois USA
                [174 ]Gusto Global LLC, Charlotte, North Carolina USA
                [175 ]GRID grid.39381.30, ISNI 0000 0004 1936 8884, Western University, ; London, Ontario Canada
                [176 ]LVDI International, San Marcos, California USA
                [177 ]GRID grid.266832.b, ISNI 0000 0001 2188 8502, University of New Mexico, ; Albuquerque, New Mexico USA
                [178 ]GRID grid.175455.7, ISNI 0000 0001 2206 1080, University of Alaska, ; Fairbanks, Alaska USA
                [179 ]GRID grid.10420.37, ISNI 0000 0001 2286 1424, University of Vienna, ; Vienna, Austria
                [180 ]GRID grid.419495.4, ISNI 0000 0001 1014 8330, Max Planck Institute for Developmental Biology, ; Tübingen, Germany
                [181 ]GRID grid.1046.3, ISNI 0000 0001 0328 1619, Australian Institute of Marine Science, ; Townsville, Queensland Australia
                [182 ]GRID grid.266093.8, ISNI 0000 0001 0668 7243, University of California Irvine, ; Irvine, California USA
                [183 ]GRID grid.264266.2, ISNI 0000 0000 9340 0716, State University of New York, ; Cortland, New York USA
                [184 ]DOCS Global, Research Triangle Park, North Carolina, USA
                [185 ]GRID grid.438526.e, ISNI 0000 0001 0694 4940, Virginia Polytechnic Institute and State University, ; Blacksburg, Virginia USA
                [186 ]GRID grid.47100.32, ISNI 0000000419368710, Yale University, ; New Haven, Connecticut USA
                [187 ]GRID grid.266685.9, ISNI 0000 0004 0386 3207, University of Massachusetts Boston, ; Boston, Massachusetts USA
                [188 ]GRID grid.495382.1, ISNI 0000 0004 1776 0452, Tongren University, ; Tongren, Guizhou China
                [189 ]GRID grid.462982.3, ISNI 0000 0000 8883 2602, University of Washington Bothell, ; Bothell, Washington USA
                [190 ]GRID grid.11480.3c, ISNI 0000000121671098, University of the Basque Country (UPV/EHU), ; Leioa, Spain
                [191 ]GRID grid.13402.34, ISNI 0000 0004 1759 700X, Zhejiang Institute of Microbiology, ; Hangzhou, Zhejiang China
                Article
                BFnature24621
                10.1038/nature24621
                6192678
                29088705
                ead59d73-50a6-4d27-80eb-b70f8a17014c
                © The Author(s) 2017

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                : 13 March 2017
                : 10 October 2017
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                environmental microbiology,microbiome
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