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      Microbial control over carbon cycling in soil

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      Frontiers in Microbiology

      Frontiers Research Foundation

      microbial communities, carbon, diversity, litter, roots, soil

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          Abstract

          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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          Most cited references 43

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          Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients

          Terrestrial ecosystems are receiving elevated inputs of nitrogen (N) from anthropogenic sources and understanding how these increases in N availability affect soil microbial communities is critical for predicting the associated effects on belowground ecosystems. We used a suite of approaches to analyze the structure and functional characteristics of soil microbial communities from replicated plots in two long-term N fertilization experiments located in contrasting systems. Pyrosequencing-based analyses of 16S rRNA genes revealed no significant effects of N fertilization on bacterial diversity, but significant effects on community composition at both sites; copiotrophic taxa (including members of the Proteobacteria and Bacteroidetes phyla) typically increased in relative abundance in the high N plots, with oligotrophic taxa (mainly Acidobacteria) exhibiting the opposite pattern. Consistent with the phylogenetic shifts under N fertilization, shotgun metagenomic sequencing revealed increases in the relative abundances of genes associated with DNA/RNA replication, electron transport and protein metabolism, increases that could be resolved even with the shallow shotgun metagenomic sequencing conducted here (average of 75 000 reads per sample). We also observed shifts in the catabolic capabilities of the communities across the N gradients that were significantly correlated with the phylogenetic and metagenomic responses, indicating possible linkages between the structure and functioning of soil microbial communities. Overall, our results suggest that N fertilization may, directly or indirectly, induce a shift in the predominant microbial life-history strategies, favoring a more active, copiotrophic microbial community, a pattern that parallels the often observed replacement of K-selected with r-selected plant species with elevated N.
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            Toward an ecological classification of soil bacteria.

            Although researchers have begun cataloging the incredible diversity of bacteria found in soil, we are largely unable to interpret this information in an ecological context, including which groups of bacteria are most abundant in different soils and why. With this study, we examined how the abundances of major soil bacterial phyla correspond to the biotic and abiotic characteristics of the soil environment to determine if they can be divided into ecologically meaningful categories. To do this, we collected 71 unique soil samples from a wide range of ecosystems across North America and looked for relationships between soil properties and the relative abundances of six dominant bacterial phyla (Acidobacteria, Bacteroidetes, Firmicutes, Actinobacteria, alpha-Proteobacteria, and the beta-Proteobacteria). Of the soil properties measured, net carbon (C) mineralization rate (an index of C availability) was the best predictor of phylum-level abundances. There was a negative correlation between Acidobacteria abundance and C mineralization rates (r2 = 0.26, P < 0.001), while the abundances of beta-Proteobacteria and Bacteroidetes were positively correlated with C mineralization rates (r2 = 0.35, P < 0.001 and r2 = 0.34, P < 0.001, respectively). These patterns were explored further using both experimental and meta-analytical approaches. We amended soil cores from a specific site with varying levels of sucrose over a 12-month period to maintain a gradient of elevated C availabilities. This experiment confirmed our survey results: there was a negative relationship between C amendment level and the abundance of Acidobacteria (r2 = 0.42, P < 0.01) and a positive relationship for both Bacteroidetes and beta-Proteobacteria (r2 = 0.38 and 0.70, respectively; P < 0.01 for each). Further support for a relationship between the relative abundances of these bacterial phyla and C availability was garnered from an analysis of published bacterial clone libraries from bulk and rhizosphere soils. Together our survey, experimental, and meta-analytical results suggest that certain bacterial phyla can be differentiated into copiotrophic and oligotrophic categories that correspond to the r- and K-selected categories used to describe the ecological attributes of plants and animals. By applying the copiotroph-oligotroph concept to soil microorganisms we can make specific predictions about the ecological attributes of various bacterial taxa and better understand the structure and function of soil bacterial communities.
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              Global-scale similarities in nitrogen release patterns during long-term decomposition.

              Litter decomposition provides the primary source of mineral nitrogen (N) for biological activity in most terrestrial ecosystems. A 10-year decomposition experiment in 21 sites from seven biomes found that net N release from leaf litter is dominantly driven by the initial tissue N concentration and mass remaining regardless of climate, edaphic conditions, or biota. Arid grasslands exposed to high ultraviolet radiation were an exception, where net N release was insensitive to initial N. Roots released N linearly with decomposition and exhibited little net N immobilization. We suggest that fundamental constraints on decomposer physiologies lead to predictable global-scale patterns in net N release during decomposition.
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                Author and article information

                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                26 September 2012
                2012
                : 3
                Affiliations
                Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara Santa Barbara, CA, USA
                Author notes

                Edited by: Diana Reid Nemergut, University of Colorado at Boulder, USA

                Reviewed by: Anthony Yannarell, University of Illinois at Urbana-Champaign, USA; Mark Bradford, Yale University, USA; Kelly Sierra Ramriez, Global Soil Biodiversity Initiative, Colorado State University, USA

                *Correspondence: Joshua P. Schimel, Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, Santa Barbara, CA 93106, USA. e-mail: schimel@ 123456lifesci.ucsb.edu

                †Current address: Sean M. Schaeffer, Department of Biosystems Engineering & Soil Science, University of Tennessee, 2506 E.J. Chapman Drive, Knoxville, TN 37996-4531, USA.

                This article was submitted to Frontiers in Terrestrial Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2012.00348
                3458434
                23055998
                Copyright © Schimel and Schaeffer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits non-commercial use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.

                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 139, Pages: 11, Words: 0
                Categories
                Microbiology
                Review Article

                Microbiology & Virology

                microbial communities, roots, carbon, soil, litter, diversity

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