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      Nutrient enrichment induces dormancy and decreases diversity of active bacteria in salt marsh sediments

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          Abstract

          Microorganisms control key biogeochemical pathways, thus changes in microbial diversity, community structure and activity can affect ecosystem response to environmental drivers. Understanding factors that control the proportion of active microbes in the environment and how they vary when perturbed is critical to anticipating ecosystem response to global change. Increasing supplies of anthropogenic nitrogen to ecosystems globally makes it imperative that we understand how nutrient supply alters active microbial communities. Here we show that nitrogen additions to salt marshes cause a shift in the active microbial community despite no change in the total community. The active community shift causes the proportion of dormant microbial taxa to double, from 45 to 90%, and induces diversity loss in the active portion of the community. Our results suggest that perturbations to salt marshes can drastically alter active microbial communities, however these communities may remain resilient by protecting total diversity through increased dormancy.

          Abstract

          Increased anthropogenic nitrogen inputs into the biosphere are fundamentally altering ecosystems worldwide. Here, Kearns et al. show that a decade of nitrogen additions to salt marshes reduces the proportion of active microorganisms, despite no net change to the total microbial community.

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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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            Swarm: robust and fast clustering method for amplicon-based studies

            Popular de novo amplicon clustering methods suffer from two fundamental flaws: arbitrary global clustering thresholds, and input-order dependency induced by centroid selection. Swarm was developed to address these issues by first clustering nearly identical amplicons iteratively using a local threshold, and then by using clusters’ internal structure and amplicon abundances to refine its results. This fast, scalable, and input-order independent approach reduces the influence of clustering parameters and produces robust operational taxonomic units.
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              Dormancy contributes to the maintenance of microbial diversity.

              Dormancy is a bet-hedging strategy used by a variety of organisms to overcome unfavorable environmental conditions. By entering a reversible state of low metabolic activity, dormant individuals become members of a seed bank, which can determine community dynamics in future generations. Although microbiologists have documented dormancy in both clinical and natural settings, the importance of seed banks for the diversity and functioning of microbial communities remains untested. Here, we develop a theoretical model demonstrating that microbial communities are structured by environmental cues that trigger dormancy. A molecular survey of lake ecosystems revealed that dormancy plays a more important role in shaping bacterial communities than eukaryotic microbial communities. The proportion of dormant bacteria was relatively low in productive ecosystems but accounted for up to 40% of taxon richness in nutrient-poor systems. Our simulations and empirical data suggest that regional environmental cues and dormancy synchronize the composition of active communities across the landscape while decoupling active microbes from the total community at local scales. Furthermore, we observed that rare bacterial taxa were disproportionately active relative to common bacterial taxa, suggesting that microbial rank-abundance curves are more dynamic than previously considered. We propose that repeated transitions to and from the seed bank may help maintain the high levels of microbial biodiversity that are observed in nearly all ecosystems.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                26 September 2016
                2016
                : 7
                : 12881
                Affiliations
                [1 ]Department of Biology, University of Massachusetts Boston , 100 Morrissey Boulevard, Boston, Massachusetts 02125, USA
                [2 ]Department of Chemistry and Geochemistry, Woods Hole Oceanographic Institution (MIT-WHOI Joint Program) , 266 Woods Hole Road, Woods Hole, Massachusetts 02543, USA
                [3 ]Ecosystems Center, Marine Biological Laboratory , 7 MBL Street, Woods Hole, Massachusetts 02543, USA
                [4 ]Department of Chemistry, Wellesley College , 106 Central Street, Wellesley, Massachusetts 02481, USA
                Author notes
                [*]

                Present address: Woods Hole Research Center, 149 Falmouth Road, Falmouth, Massachusetts 02540, USA

                [†]

                Present address: Department of Marine and Environmental Science, Marine Science Center, Northeastern University, 430 Nahant Road, Nahant, Massachusetts 01908, USA

                Article
                ncomms12881
                10.1038/ncomms12881
                5052679
                27666199
                29e9169c-bca9-442d-aa87-79ab1c2174aa
                Copyright © 2016, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 14 January 2016
                : 10 August 2016
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