On Copiotrophy and Temperature: Controls on Microbial Maximum Growth Rate Versus Translation Rate Optimization

Maximum growth rate is often used as a primary axis of functional variation in studies of microorganisms because it is key parameter in models of microbial growth, because it is closely conceptually related to the “copiotrophy-oligotrophy” axis used to organize microbial functional roles within ecosystems, and because emerging tools make it straightforward to estimate from genomic and metagenomic data. However, temperature, via its influence on reaction kinetics, may act as a confounder in studies that measure genomic signatures of growth optimization across environments by decoupling the cellular optimization for relatively fast growth from absolute growth rates. Observations suggest that growth optimization need not always indicate rapid growth. For example, strong temperature gradients are the norm across much of the world’s oceans, where slow-growing deep-ocean microbes show elevated signals of genomic growth optimization relative to the faster-growing communities at the surface. Looking across environments, we find a negative relationship between genomic growth optimization and optimal growth temperature, indicating the potential decoupling of genomic traits associated with copiotrophy from maximum growth rate, particularly when measured in the presence of a strong temperature gradient. Our results suggest that, as a result of temperature’s confounding effects, genomic signatures of growth optimization better predict the ecological roles and functional genomic content of microorganisms than do growth rates themselves. Finally, we suggest reframing copiotrophy as a set of traits that allow an organism to escape from a thermodynamic baseline maximum growth rate, rather than in relation to a specific rate cutoff.