Beyond Growth: The Significance of Non-Growth Anabolism for Microbial Carbon-Use Efficiency in the Light of Soil Carbon Stabilisation
2023
Bölscher, Tobias | Vogel, Cordula | Olagoke, Folasade | Meurer, Katharina H.E. | Herrmann, Anke | Colombi, Tino | Brunn, Melanie | Domeignoz-Horta, Luiz | Ecologie fonctionnelle et écotoxicologie des agroécosystèmes (ECOSYS) ; AgroParisTech-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) | Technische Universität Dresden = Dresden University of Technology (TU Dresden) | Swedish University of Agricultural Sciences = Sveriges lantbruksuniversitet (SLU) | University of Koblenz-Landau | Universität Zürich [Zürich] = University of Zurich (UZH) | This work was supported by Agence National de la Recherche (ANR-20-IDEES-0002), the Deutsche Forschungsgemeinschaft (DFG, Bonn, Germany under the grant VO 2111/4-1), the Swedish Research Council for Sustainable Development (Formas 2019-01189) and the EU EJP SOIL project EnergyLink (“Linking crop diversification to microbial energy allocation and organic carbon storage in soils”) within the European Union Horizon 2020 research and innovation programme (Grant Agreement No. 862695, EJP SOIL).
Microbial carbon-use efficiency (CUE) in soils captures carbon (C) partitioning between anabolic biosynthesis of microbial metabolites and catabolic C emissions (i.e. respiratory C waste). The use of C for biosynthesis provides a potential for the accumulation of microbial metabolic residues in soil. Recognized as a crucial control in C cycling, microbial CUE is implemented in the majority of soil C models. Due to the models’ high sensitivity to CUE, reliable soil C projections demand accurate CUE quantifications. Current measurements of CUE neglect microbial non-growth metabolites, such as extracellular polymeric substances (EPS) or exoenzymes, although they remain in soil and could be quantitatively important. Here, we highlight that disregarding non-growth anabolism can lead to severe underestimations of CUE. Based on two case studies, we demonstrate that neglecting exoenzyme and EPS production underestimates CUE by more than 100% and up to 30%, respectively. Using these values in model simulations, we observed that the model projects up to 34% larger SOC stocks when non-growth metabolites are considered for estimating CUE. Our considerations outlined here challenge the current ways how CUE is measured. Research efforts should focus on (i) advancing CUE estimations by capturing the multitude of microbial C uses, (ii) improving techniques to quantify non-growth metabolic products in soil, and (iii) providing an understanding of dynamic metabolic C uses under different environmental conditions and over time. In the light of current discussion on soil C stabilization mechanisms, we call for efforts to open the ‘black box’ of microbial physiology in soil and to incorporate all quantitative important C uses in CUE measurements.
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