Beyond Growth: The Significance of Non-Growth Anabolism for Microbial Carbon-Use Efficiency in the Light of Soil Carbon Stabilisation

Abstract

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. Recognised 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. By incorporating these case-specific values in model simulations, we observed that the model projects up to 34% larger SOC stocks over a period of 64 years when non-growth metabolites are considered for estimating CUE, highlighting the crucial importance of accurate CUE quantification. Our considerations outlined here challenge the current ways how CUE is measured and we suggest improvements concerning the quantification of non-growth metabolites. 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 stabilisation 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.

Keywords: microbial growth efficiency, substrate-use efficiency, microbial physiology, non-growth metabolism, microbial exudates, soil carbon models