Resource identity and taxonomy hierarchically structure bacterial growth efficiency

Bacterial metabolism sustains the biosphere by driving planetary elemental cycles. For example, CO₂ production during bacterial respiration of organic carbon is a key process in the global carbon cycle. Bacterial CO₂ production depends on the allocation of carbon between biomass production and energy generation. This allocation is quantified by the bacterial growth efficiency (BGE)—the fraction of utilized carbon converted to biomass. BGE is a key trait that determines the balance between cellular growth and energetic demands. However, we do not yet understand how BGE depends on the carbon source, growth rate, or taxonomy. This gap arises from a lack of quantitative measurements of CO₂ production and biomass across diverse bacteria.

We address this challenge using a new high-throughput platform that directly quantifies dynamic CO₂ production and carbon accumulation in biomass. We measured BGE and growth rate for ~20 taxa across three dominant soil phyla on glycolytic (glucose) and gluconeogenic (succinate) substrates. We find no global correlation between BGE and growth rate—a result supported by a simple theoretical model. We show that BGE is structured hierarchically: first by resource, with higher efficiency on glucose than on succinate; and then by phylum, with Actinobacteria highest on both resources and Bacillota lowest.

In addition, we characterize diverse dynamic patterns of CO₂ production during growth, potentially reflecting overflow metabolism. We explore the relationships among these dynamic traits, BGE, and genomic variation. Our results suggest that understanding carbon cycling in microbial communities requires delineating the effects of resource identity and taxonomy on metabolic traits.