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      Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in Western Siberia

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          Abstract

          Soil horizons below 30 cm depth contain about 60% of the organic carbon stored in soils. Although insight into the physical and chemical stabilization of soil organic matter (SOM) and into microbial community composition in these horizons is being gained, information on microbial functions of subsoil microbial communities and on associated microbially-mediated processes remains sparse. To identify possible controls on enzyme patterns, we correlated enzyme patterns with biotic and abiotic soil parameters, as well as with microbial community composition, estimated using phospholipid fatty acid profiles. Enzyme patterns (i.e. distance-matrixes calculated from these enzyme activities) were calculated from the activities of six extracellular enzymes (cellobiohydrolase, leucine-amino-peptidase, N-acetylglucosaminidase, chitotriosidase, phosphatase and phenoloxidase), which had been measured in soil samples from organic topsoil horizons, mineral topsoil horizons, and mineral subsoil horizons from seven ecosystems along a 1500 km latitudinal transect in Western Siberia. We found that hydrolytic enzyme activities decreased rapidly with depth, whereas oxidative enzyme activities in mineral horizons were as high as, or higher than in organic topsoil horizons. Enzyme patterns varied more strongly between ecosystems in mineral subsoil horizons than in organic topsoils. The enzyme patterns in topsoil horizons were correlated with SOM content (i.e., C and N content) and microbial community composition. In contrast, the enzyme patterns in mineral subsoil horizons were related to water content, soil pH and microbial community composition. The lack of correlation between enzyme patterns and SOM quantity in the mineral subsoils suggests that SOM chemistry, spatial separation or physical stabilization of SOM rather than SOM content might determine substrate availability for enzymatic breakdown. The correlation of microbial community composition and enzyme patterns in all horizons, suggests that microbial community composition shapes enzyme patterns and might act as a modifier for the usual dependency of decomposition rates on SOM content or C/N ratios.

          Highlights

          • Enzyme patterns differed more strongly between horizons than between ecosystems.

          • Enzyme patterns in subsoils vary more strongly than enzyme patterns in topsoils.

          • Enzyme patterns in topsoil are related to SOM content and mic. community composition.

          • Enzyme patterns in mineral subsoil were not related to SOM content or SOM C/N.

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          Most cited references55

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          Stoichiometry of soil enzyme activity at global scale.

          Extracellular enzymes are the proximate agents of organic matter decomposition and measures of these activities can be used as indicators of microbial nutrient demand. We conducted a global-scale meta-analysis of the seven-most widely measured soil enzyme activities, using data from 40 ecosystems. The activities of beta-1,4-glucosidase, cellobiohydrolase, beta-1,4-N-acetylglucosaminidase and phosphatase g(-1) soil increased with organic matter concentration; leucine aminopeptidase, phenol oxidase and peroxidase activities showed no relationship. All activities were significantly related to soil pH. Specific activities, i.e. activity g(-1) soil organic matter, also varied in relation to soil pH for all enzymes. Relationships with mean annual temperature (MAT) and precipitation (MAP) were generally weak. For hydrolases, ratios of specific C, N and P acquisition activities converged on 1 : 1 : 1 but across ecosystems, the ratio of C : P acquisition was inversely related to MAP and MAT while the ratio of C : N acquisition increased with MAP. Oxidative activities were more variable than hydrolytic activities and increased with soil pH. Our analyses indicate that the enzymatic potential for hydrolyzing the labile components of soil organic matter is tied to substrate availability, soil pH and the stoichiometry of microbial nutrient demand. The enzymatic potential for oxidizing the recalcitrant fractions of soil organic material, which is a proximate control on soil organic matter accumulation, is most strongly related to soil pH. These trends provide insight into the biogeochemical processes that create global patterns in ecological stoichiometry and organic matter storage.
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            Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil

            Plant seasonal cycles alter carbon (C) and nitrogen (N) availability for soil microbes, which may affect microbial community composition and thus feed back on microbial decomposition of soil organic material and plant N availability. The temporal dynamics of these plant–soil interactions are, however, unclear. Here, we experimentally manipulated the C and N availability in a beech forest through N fertilization or tree girdling and conducted a detailed analysis of the seasonal pattern of microbial community composition and decomposition processes over 2 yr. We found a strong relationship between microbial community composition and enzyme activities over the seasonal course. Phenoloxidase and peroxidase activities were highest during late summer, whereas cellulase and protease peaked in late autumn. Girdling, and thus loss of mycorrhiza, resulted in an increase in soil organic matter-degrading enzymes and a decrease in cellulase and protease activity. Temporal changes in enzyme activities suggest a switch of the main substrate for decomposition between summer (soil organic matter) and autumn (plant litter). Our results indicate that ectomycorrhizal fungi are possibly involved in autumn cellulase and protease activity. Our study shows that, through belowground C allocation, trees significantly alter soil microbial communities, which may affect seasonal patterns of decomposition processes.
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              Microbial community dynamics alleviate stoichiometric constraints during litter decay

              Under the current paradigm, organic matter decomposition and nutrient cycling rates are a function of the imbalance between substrate and microbial biomass stoichiometry. Challenging this view, we demonstrate that in an individual-based model, microbial community dynamics alter relative C and N limitation during litter decomposition, leading to a system behaviour not predictable from stoichiometric theory alone. Rather, the dynamics of interacting functional groups lead to an adaptation at the community level, which accelerates nitrogen recycling in litter with high initial C : N ratios and thus alleviates microbial N limitation. This mechanism allows microbial decomposers to overcome large imbalances between resource and biomass stoichiometry without the need to decrease carbon use efficiency (CUE), which is in contrast to predictions of traditional stoichiometric mass balance equations. We conclude that identifying and implementing microbial community-driven mechanisms in biogeochemical models are necessary for accurately predicting terrestrial C fluxes in response to changing environmental conditions.
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                Author and article information

                Contributors
                Journal
                Soil Biol Biochem
                Soil Biol. Biochem
                Soil Biology & Biochemistry
                Pergamon Press
                0038-0717
                1 April 2015
                April 2015
                : 83
                : 106-115
                Affiliations
                [a ]University of Vienna, Department of Microbiology and Ecosystem Science, Division of Terrestrial Ecosystem Research, Vienna, Austria
                [b ]Austrian Polar Research Institute, Vienna, Austria
                [c ]University of Vienna, Department of Ecogenomics and Systems Biology, Division of Archaea Biology and Ecogenomics, Vienna, Austria
                [d ]Leibniz Universität Hannover, Institut für Bodenkunde, Hannover, Germany
                [e ]Aarhus University, Center for Geomicrobiology, Department of Bioscience, Aarhus, Denmark
                [f ]University of Bergen, Centre for Geobiology, Bergen, Norway
                [g ]Central Siberian Botanical Garden, Siberian Branch of Russian Academy of Sciences, Novosibirsk, Russia
                Author notes
                []Corresponding author. University of Vienna, Department of Microbiology and Ecosystem Science, Division of Terrestrial Ecosystem Research, Althanstraße 14, Vienna, 1090, Austria. Tel.: +43 1 4277 76668; fax: +43 1 4277 876661. joerg.schnecker@ 123456univie.ac.at
                Article
                S0038-0717(15)00028-0
                10.1016/j.soilbio.2015.01.016
                4381299
                25859057
                fb46ff8b-dc13-416c-8fd4-a22082b1341b
                © 2015 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 29 September 2014
                : 10 January 2015
                : 16 January 2015
                Categories
                Article

                Microbiology & Virology
                extracellular enzymes,plfa,tundra,boreal forests,steppe,permafrost
                Microbiology & Virology
                extracellular enzymes, plfa, tundra, boreal forests, steppe, permafrost

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