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      Resuscitation of the rare biosphere contributes to pulses of ecosystem activity

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          Abstract

          Dormancy is a life history trait that may have important implications for linking microbial communities to the functioning of natural and managed ecosystems. Rapid changes in environmental cues may resuscitate dormant bacteria and create pulses of ecosystem activity. In this study, we used heavy-water (H 18 2O) stable isotope probing (SIP) to identify fast-growing bacteria that were associated with pulses of trace gasses (CO 2, CH 4, and N 2O) from different ecosystems [agricultural site, grassland, deciduous forest, and coniferous forest (CF)] following a soil-rewetting event. Irrespective of ecosystem type, a large fraction (69–74%) of the bacteria that responded to rewetting were below detection limits in the dry soils. Based on the recovery of sequences, in just a few days, hundreds of rare taxa increased in abundance and in some cases became dominant members of the rewetted communities, especially bacteria belonging to the Sphingomonadaceae, Comamonadaceae, and Oxalobacteraceae. Resuscitation led to dynamic shifts in the rank abundance of taxa that caused previously rare bacteria to comprise nearly 60% of the sequences that were recovered in rewetted communities. This rapid turnover of the bacterial community corresponded with a 5–20-fold increase in the net production of CO 2 and up to a 150% reduction in the net production of CH 4 from rewetted soils. Results from our study demonstrate that the rare biosphere may account for a large and dynamic fraction of a community that is important for the maintenance of bacterial biodiversity. Moreover, our findings suggest that the resuscitation of rare taxa from seed banks contribute to ecosystem functioning.

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          Benefits of plant diversity to ecosystems: immediate, filter and founder effects

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            Beyond the Venn diagram: the hunt for a core microbiome.

            Discovering a core microbiome is important for understanding the stable, consistent components across complex microbial assemblages. A core is typically defined as the suite of members shared among microbial consortia from similar habitats, and is represented by the overlapping areas of circles in Venn diagrams, in which each circle contains the membership of the sample or habitats being compared. Ecological insight into core microbiomes can be enriched by 'omics approaches that assess gene expression, thereby extending the concept of the core beyond taxonomically defined membership to community function and behaviour. Parameters defined by traditional ecology theory, such as composition, phylogeny, persistence and connectivity, will also create a more complex portrait of the core microbiome and advance understanding of the role of key microorganisms and functions within and across ecosystems. © 2011 Society for Applied Microbiology and Blackwell Publishing Ltd.
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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

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                30 January 2015
                2015
                : 6
                : 24
                Affiliations
                [1] 1Department of Plant and Wildlife Sciences, Brigham Young University Provo, UT, USA
                [2] 2Department of Biological Sciences, University of Notre Dame South Bend, IN, USA
                [3] 3Department of Ecology and Evolutionary Biology and CIRES, University of Colorado Boulder, CO, USA
                [4] 4Cooperative Institute for Research in Environmental Sciences, University of Colorado Boulder, CO, USA
                [5] 5Department of Biology, Indiana University Bloomington, IN, USA
                Author notes

                Edited by: Jérôme Comte, Laval University, Canada

                Reviewed by: Pierre E. Galand, Observatoire Océanologique de Banyuls, France; Ramiro Logares, Spanish National Research Council (CSIC), Spain

                *Correspondence: Jay T. Lennon, Department of Biology, Indiana University, 1001 E. 3rd St., Bloomington, IN 47405, USA e-mail: lennonj@ 123456indiana.edu

                This article was submitted to Terrestrial Microbiology, a section of the journal Frontiers in Microbiology.

                Article
                10.3389/fmicb.2015.00024
                4311709
                25688238
                4e259d87-ecf1-4087-87da-3c8d3d82e25f
                Copyright © 2015 Aanderud, Jones, Fierer and Lennon.

                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
                : 14 October 2014
                : 08 January 2015
                Page count
                Figures: 6, Tables: 0, Equations: 1, References: 74, Pages: 11, Words: 8802
                Categories
                Microbiology
                Original Research Article

                Microbiology & Virology
                co2 pulses,dormancy,desiccation,dominance,stable isotope probing (sip),soil rewetting,seed bank,rarity

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