Beyond growth? The significance of microbial maintenance for carbon-use efficiency in the light of soil carbon storage

During decomposition of organic matter, soil microbes determine the fate of C. They partition C between anabolic biosynthesis of various new microbial metabolites (i.e. C reuse) and catabolic C emissions (i.e. C waste, mainly through respiration). This partitioning is commonly referred to as microbial carbon-use efficiency (CUE). The reuse of C during biosynthesis provides a potential for the accumulation of microbial metabolic residues in soil. The microbial metabolic performance is a key factor in soil C dynamics, because the vast majority of C inputs to soil will – sooner or later – be processed by soil microorganisms. Soil C inputs will thus be subjected to microbial allocation of C towards reuse or emitted waste, with the former leading to C remaining in soil. Recognized as a crucial control in C cycling, microbial CUE is implemented – implicitly or explicitly – in soil C models, which react highly sensitive to even small changes in CUE. Due to the models’ high sensitivity, reliable soil C projections demand accurate CUE quantifications, capturing unambiguously all metabolic C fluxes.

The current concept of microbial CUE neglects microbial maintenance which could make up considerable parts of the microbially processed C. Commonly, CUE is quantified from C incorporated into biomass or used for growth and C released as CO₂. Extracellular metabolites, such as polymeric substances (EPS), exoenzymes or nutrient mobilizing compounds, as well as intracellular maintenance metabolites, such as storage compounds or endoenzymes, are ignored although they represent microbial metabolic C reuse and thus C remaining in soil.

Based on theoretical considerations and a case study for EPS production, we will demonstrate that neglecting microbial maintenance can have severe impact on estimation of terrestrial C storage. For instance, ignoring measured EPS production (of a quantity of C which equals 37 % of the C used for growth) causes a substantial underestimation of CUE. Here, current approaches of CUE provide an apparent CUE of 0.20 while disregard an actual CUE of 0.25 (i.e. CUE is 25 % higher when maintenance metabolism is considered). Based on our findings, we suggest an adjustment of how we conceptualize and calculate microbial CUE in soils.