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

Maximum growth rates are often included as a major axis of functional variation in comparative studies because they are straightforward to estimate from genomic and metagenomic data, because they represent key parameters in models of microbial growth, and because maximum growth rate is closely conceptually related to the “copiotrophy-oligotrophy” axis used by many to organize microbial functional roles within ecosystems. Most methods to genomically estimate growth maxima include a temperature correction that accounts for the fact that organisms will grow faster at higher temperatures due to underlying reaction kinetics. Yet, this correction implies 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 appear to show elevated signals of genomic growth optimization relative to the faster-growing communities at the surface. Looking across environments, we show how a negative relationship between genomic growth optimization and optimal growth temperature leads to a decoupling of the relationship between genomic traits associated with copiotrophy and observed maximum growth rates when measured in the presence of a strong temperature gradient. We go on to show 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.