Respiration by soil bacteria and fungi is one of the largest fluxes of carbon (C) from the land surface, producing 78-98 Pg C/yr in the form of CO2. Although this flux is a direct product of microbial metabolism, controls over metabolism and their responses to global change are a major uncertainty in the global C cycle. A single, constant parameter, carbon use efficiency (CUE), is often used in models to determine the partitioning of C between losses as respiration and incorporation into microbial biomass, which can ultimately enter the soil organic C pool. This parameter has a large impact on estimates and projections of soil C pool sizes and greenhouse gas emissions from soil; however, it is not well-understood how CUE varies between bacterial taxa and whether this variation makes microbial community composition an important factor in predicting C cycle fluxes. We developed a novel, in silico approach to estimate bacterial C-use efficiency (CUE) for over 200 taxa using genome-scale constraint-based metabolic modeling. Additionally, we incorporate the range of CUE values we observed across taxa into an existing soil biogeochemical model to estimate the impact of physiological variation between taxa on C cycle fluxes.
Results/Conclusions
Intrinsic physiological variation among taxa results in >300% variation in CUE (0.2-0.9). These differences among taxa can alter estimates of soil C emissions as strongly as seasonal or latitudinal changes in temperature when incorporated into a biogeochemical model. We also find that CUE has a significant phylogenetic signal, with variation among taxa structured primarily at the class and order levels. CUE is negatively correlated with GC content and with genome size. However, taxa with larger genomes were able to access a wider range of metabolites, suggesting a fundamental tradeoff between efficiency and survivorship in fluctuating environments. Under metabolite replete conditions, mean potential CUE is 0.62 ± 0.17 whereas metabolite-limiting conditions characteristic of field conditions decrease CUE to 0.29 ± 0.19. When metabolite diversity is altered under global change specialist bacterial taxa with small, C-use efficient genomes may be replaced by generalist taxa with larger genomes whose CO2 emissions enhance anthropogenic feedbacks to climate change. The relationships we observe here between microbial community composition, bacterial physiology, and C cycling provide a means for improving the mechanistic representation of microbial processes in C cycle models.