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      Microbial control over carbon cycling in soil

      research-article
      ,
      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 references43

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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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            Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization.

            The influence of pH on the relative importance of the two principal decomposer groups in soil, fungi and bacteria, was investigated along a continuous soil pH gradient at Hoosfield acid strip at Rothamsted Research in the United Kingdom. This experimental location provides a uniform pH gradient, ranging from pH 8.3 to 4.0, within 180 m in a silty loam soil on which barley has been continuously grown for more than 100 years. We estimated the importance of fungi and bacteria directly by measuring acetate incorporation into ergosterol to measure fungal growth and leucine and thymidine incorporation to measure bacterial growth. The growth-based measurements revealed a fivefold decrease in bacterial growth and a fivefold increase in fungal growth with lower pH. This resulted in an approximately 30-fold increase in fungal importance, as indicated by the fungal growth/bacterial growth ratio, from pH 8.3 to pH 4.5. In contrast, corresponding effects on biomass markers for fungi (ergosterol and phospholipid fatty acid [PLFA] 18:2omega6,9) and bacteria (bacterial PLFAs) showed only a two- to threefold difference in fungal importance in the same pH interval. The shift in fungal and bacterial importance along the pH gradient decreased the total carbon mineralization, measured as basal respiration, by only about one-third, possibly suggesting functional redundancy. Below pH 4.5 there was universal inhibition of all microbial variables, probably derived from increased inhibitory effects due to release of free aluminum or decreasing plant productivity. To investigate decomposer group importance, growth measurements provided significantly increased sensitivity compared with biomass-based measurements.
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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
                : 348
                Affiliations
                simpleDepartment 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
                67718d5f-2bdb-4dc8-ba75-22e75e3f50ec
                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.

                History
                : 25 June 2012
                : 09 September 2012
                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
                Microbiology & Virology
                microbial communities, roots, carbon, soil, litter, diversity

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