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      Significance of microbial asynchronous anabolism to soil carbon dynamics driven by litter inputs

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      1 , a , 1 , 2
      Scientific Reports
      Nature Publishing Group

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          Abstract

          Soil organic carbon (SOC) plays an important role in the global carbon cycle. However, it remains largely unknown how plant litter inputs impact magnitude, composition and source configuration of the SOC stocks over long term through microbial catabolism and anabolism, mostly due to uncoupled research on litter decomposition and SOC formation. This limits our ability to predict soil system responses to changes in land-use and climate. Here, we examine how microbes act as a valve controlling carbon sequestrated from plant litters versus released to the atmosphere in natural ecosystems amended with plant litters varying in quantity and quality. We find that litter quality – not quantity – regulates long-term SOC dynamics under different plausible scenarios. Long-term changes in bulk SOC stock occur only when the quality of carbon inputs causes asynchronous change in a microbial physiological trait, defined as “microbial biosynthesis acceleration” (MBA). This is the first theoretical demonstration that the response of the SOC stocks to litter inputs is critically determined by the microbial physiology. Our work suggests that total SOC at an equilibrium state may be an intrinsic property of a given ecosystem, which ultimately is controlled by the asynchronous MBA between microbial functional 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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            Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function.

            Advances in spectroscopic and other chemical methods have greatly enhanced our ability to characterize soil organic matter chemistry. As a result, the molecular characteristics of soil C are now known for a range of ecosystems, soil types, and management intensities. Placing this knowledge into a broader ecological and management context is difficult, however, and remains one of the fundamental challenges of soil organic matter research. Here we present a conceptual model of molecular soil C dynamics to stimulate inter-disciplinary research into the ecological implications of molecular C turnover and its management- and process-level controls. Our model describes three properties of soil C dynamics: 1) soil size fractions have unique molecular patterns that reflect varying degrees of biological and physical control over decomposition; 2) there is a common decomposition sequence independent of plant inputs or other ecosystem properties; and 3) molecular decomposition sequences, although consistent, are not uniform and can be altered by processes that accelerate or slow the microbial transformation of specific molecules. The consequences of this model include several key points. First, lignin presents a constraint to decomposition of plant litter and particulate C (>53 microm) but exerts little influence on more stable mineral-associated soil fractions <53 microm. Second, carbon stabilized onto mineral fractions has a distinct composition related more to microbially processed organic matter than to plant-related compounds. Third, disturbances, such as N fertilization and tillage, which alter decomposition rates, can have "downstream effects"; that is, a disturbance that directly alters the molecular dynamics of particulate C may have a series of indirect effects on C stabilization in silt and clay fractions.
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              Microbially derived inputs to soil organic matter: are current estimates too low?

              Soil microbes are central to many soil processes, but due to the structural complexity of soil organic matter, the accurate quantification of microbial biomass contributions continues to pose a significant analytical challenge. In this study, microbes from a range of soils were cultured such that their molecular profile could be compared to that of soil organic matter and native vegetation. With the use of modern NMR spectroscopy, the contributions from microbial species can be discerned in soil organic matter and quantified. On the basis of these studies, the contributions of microbial biomass to soil organic matter appear to be much higher than the 1-5% reported by other researchers. In some soils, microbial biomass was found to contribute >50% of the extractable soil organic matter fractions and approximately 45% of the humin fraction and accounted for >80% of the soil nitrogen. These findings are significant because organic matter is intimately linked to nutrient release and transport in soils, nitrogen turnover rates, contaminant fate, soil quality, and fertility. Therefore, if in some cases soil organic matter and soil organic nitrogen are predominately of microbial origin, it is likely that this fraction, whether in the form of preserved material or living cells, plays an underestimated role in several soil processes.
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                Author and article information

                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group
                2045-2322
                02 April 2015
                2015
                : 5
                : 9575
                Affiliations
                [1 ]Biosciences Division, Argonne National Laboratory , Argonne, IL 60439, USA
                [2 ]State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences , Shenyang 110164, China
                Author notes
                [*]

                These two authors contributed equally to this work.

                Article
                srep09575
                10.1038/srep09575
                4387914
                25849864
                671a7832-b3d4-4116-99c0-715997bbf5a9
                Copyright © 2015, Macmillan Publishers Limited. All rights reserved

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder in order to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/4.0/

                History
                : 22 December 2014
                : 09 March 2015
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