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      Drought Legacy Effects on the Composition of Soil Fungal and Prokaryote Communities

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          Abstract

          It is increasingly acknowledged that climate change is influencing terrestrial ecosystems by increased drought and rainfall intensities. Soil microbes are key drivers of many processes in terrestrial systems and rely on water in soil pores to fulfill their life cycles and functions. However, little is known on how drought and rainfall fluctuations, which affect the composition and structure of microbial communities, persist once original moisture conditions have been restored. Here, we study how simulated short-term drying and re-wetting events shape the community composition of soil fungi and prokaryotes. In a mesocosm experiment, soil was exposed to an extreme drought, then re-wetted to optimal moisture (50% WHC, water holding capacity) or to saturation level (100% WHC). Composition, community structure and diversity of microbes were measured by sequencing ITS and 16S rRNA gene amplicons 3 weeks after original moisture content had been restored. Drying and extreme re-wetting decreased richness of microbial communities, but not evenness. Abundance changes were observed in only 8% of prokaryote OTUs, and 25% of fungal OTUs, whereas all other OTUs did not differ between drying and re-wetting treatments. Two specific legacy response groups (LRGs) were observed for both prokaryotes and fungi. OTUs belonging to the first LRG decreased in relative abundance in soil with a history of drought, whereas OTUs that increased in soil with a history of drought formed a second LRG. These microbial responses were spread among different phyla. Drought appeared to be more important for the microbial community composition than the following extreme re-wetting. 16S profiles were correlated with both inorganic N concentration and basal respiration and ITS profiles correlated with fungal biomass. We conclude that a drying and/or an extreme re-wetting history can persist in soil microbial communities via specific response groups composed of members with broad phylogenetic origins, with possible functional consequences on soil processes and plant species. As a large fraction of OTUs responding to drying and re-wetting belonged to the rare biosphere, our results suggest that low abundant microbial species are potentially important for ecosystem responses to extreme weather events.

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          Most cited references71

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          Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data

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            Examining the global distribution of dominant archaeal populations in soil.

            Archaea, primarily Crenarchaeota, are common in soil; however, the structure of soil archaeal communities and the factors regulating their diversity and abundance remain poorly understood. Here, we used barcoded pyrosequencing to comprehensively survey archaeal and bacterial communities in 146 soils, representing a multitude of soil and ecosystem types from across the globe. Relative archaeal abundance, the percentage of all 16S rRNA gene sequences recovered that were archaeal, averaged 2% across all soils and ranged from 0% to >10% in individual soils. Soil C:N ratio was the only factor consistently correlated with archaeal relative abundances, being higher in soils with lower C:N ratios. Soil archaea communities were dominated by just two phylotypes from a constrained clade within the Crenarchaeota, which together accounted for >70% of all archaeal sequences obtained in the survey. As one of these phylotypes was closely related to a previously identified putative ammonia oxidizer, we sampled from two long-term nitrogen (N) addition experiments to determine if this taxon responds to experimental manipulations of N availability. Contrary to expectations, the abundance of this dominant taxon, as well as archaea overall, tended to decline with increasing N. This trend was coupled with a concurrent increase in known N-oxidizing bacteria, suggesting competitive interactions between these groups.
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              Microbial control over carbon cycling in soil

              A major thrust of terrestrial microbial ecology is focused on understanding when and how the composition of the microbial community affects the functioning of biogeochemical processes at the ecosystem scale (meters-to-kilometers and days-to-years). While research has demonstrated these linkages for physiologically and phylogenetically “narrow” processes such as trace gas emissions and nitrification, there is less conclusive evidence that microbial community composition influences the “broad” processes of decomposition and organic matter (OM) turnover in soil. In this paper, we consider how soil microbial community structure influences C cycling. We consider the phylogenetic level at which microbes form meaningful guilds, based on overall life history strategies, and suggest that these are associated with deep evolutionary divergences, while much of the species-level diversity probably reflects functional redundancy. We then consider under what conditions it is possible for differences among microbes to affect process dynamics, and argue that while microbial community structure may be important in the rate of OM breakdown in the rhizosphere and in detritus, it is likely not important in the mineral soil. In mineral soil, physical access to occluded or sorbed substrates is the rate-limiting process. Microbial community influences on OM turnover in mineral soils are based on how organisms allocate the C they take up – not only do the fates of the molecules differ, but they can affect the soil system differently as well. For example, extracellular enzymes and extracellular polysaccharides can be key controls on soil structure and function. How microbes allocate C may also be particularly important for understanding the long-term fate of C in soil – is it sequestered or not?
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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
                07 March 2018
                2018
                : 9
                : 294
                Affiliations
                [1] 1Microbial Ecology, Department of Biology, Lund University , Lund, Sweden
                [2] 2Sections of Microbiology and Terrestrial Ecology, Department of Biology, University of Copenhagen , Copenhagen, Denmark
                [3] 3Department of Microbial Ecology, Netherlands Institute of Ecology , Wageningen, Netherlands
                [4] 4Agroécologie, UMR1347, INRA Centre Dijon , Dijon, France
                [5] 5Department of Terrestrial Ecology, Netherlands Institute of Ecology , Wageningen, Netherlands
                [6] 6Theoretical Biology and Bioinformatics, Utrecht University , Utrecht, Netherlands
                [7] 7Laboratory of Nematology, Wageningen University , Wageningen, Netherlands
                Author notes

                Edited by: Martin Hartmann, Swiss Federal Institute for Forest, Snow and Landscape Research, Switzerland

                Reviewed by: Zachary B. Freedman, West Virginia University, United States; Barbara Drigo, University of South Australia, Australia; Julie Royann Deslippe, Victoria University of Wellington, New Zealand

                *Correspondence: Annelein Meisner, Annelein.Meisner@ 123456biol.lu.se

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

                Article
                10.3389/fmicb.2018.00294
                5845876
                29563897
                77e589e3-78ed-4c2c-8d35-deb6f993d1ea
                Copyright © 2018 Meisner, Jacquiod, Snoek, ten Hooven and van der Putten.

                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) and the copyright owner 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
                : 06 November 2017
                : 08 February 2018
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 95, Pages: 12, Words: 0
                Funding
                Funded by: Vetenskapsrådet 10.13039/501100004359
                Award ID: 330-2014-6430
                Funded by: European Research Council 10.13039/501100000781
                Award ID: ERC-Adv grant 26055290
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                climate change,soil,birch effect,re-wetting,bacteria,fungi,microbial communities
                Microbiology & Virology
                climate change, soil, birch effect, re-wetting, bacteria, fungi, microbial communities

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