The carbon use efficiency paradox: why what we measure is not what we need

The pivotal role of the soil microbiome in global biogeochemical cycles is undisputed. The subsequent demand for simplified quantitative descriptions of its functions in modelling approaches resulted in transferring the pure-culture based microbial yield concept into microbial carbon use efficiency (CUE) – a “one-number” approach to partition C input to soils and to describe the physiological efficiency of the microbiome.

The holy grail lost its sanctity once our challenges to reliably determine it became evident. The method comparison of Geyer et al. (2019) identified which critical assumptions underly the contrasting outcomes in CUEs derived from these methods. Our own data just underline this: While substrate-based CUE has a temporal and substrate dependency, ¹⁸O-based and metabolic CUE remain often unaffected by substrate addition but cover, with either DNA-replication or anabolic precursor-based upscaling of biomass C formation contrasting physiological processes of microbial cells.

Such divergent findings highlight that despite decades of research, current methods do not allow an unambiguous quantification of microbial substrate use in soils, owing to two overlapping methodological challenges: 1) Neither extracting microbial biomass nor predicting it from de-novo formed DNA can deliver a reliable quantitative estimation of the newly formed microbial biomass carbon; and 2) Whatever we add as substrate to soils does not reflect what microbes use for growth under native conditions. Our progress in quantitatively covering an increasing number of cellular pools (e.g. also considering cell walls and membranes), the increased consideration of storage, and first concepts on how to integrate secreted extracellular carbon offer perspectives to tackle the first of the two challenges. However, experimentally representing the incredible diversity of organic molecules accessible to microbes for consumption in soils is yet rather avoided, although Lehmann et al (2020) postulated compound diversity as a central factor determining the fate of carbon in soils. Comparing incubations with individual compounds to those of complex monomer mixture revealed that the microbial use of an individual compounds is significantly affected by the presence or absence of other compounds, i.e. the molecular diversity in soil solution. This can readily be explained by viewing microbes through the lens of their metabolic capacities, which impose fundamental constraints on their functioning. Formation of microbial biomass requires a defined ratio of precursor building blocks, which are products of distinct pathways of the basic carbon metabolism. De-novo production requires expression and formation of all pathway-related enzymes, while direct precursor uptake from soil solution allows for “saving” this energy. Therefore, we postulate that monomer diversity would positively affect microbial efficiency. This may be contrasting for polymer diversity, where extracellular enzyme costs exceed those of intracellular de-novo formation and thus a low diversity may be bioenergetically favorable. Thus, substrate diversity-efficiency relationships may centrally underlie deviations between our current CUE approaches. We recommend microbial ecologists to whenever possible replace CUE by the actual processes of interest, i.e. the ecophysiological response and subsequent changes in microbial pools (metabolome, growth) and fluxes (fluxome). This would provide parameters allowing for quantitative upscaling to pools and fluxes required for higher scale soil system models.