Mechanistic model of nutrient uptake explains dichotomy between marine oligotrophic and copiotrophic bacteria

Marine bacterial diversity is immense and believed to be driven in part by trade-offs in metabolic strategies. Here we consider heterotrophs that rely on organic carbon as an energy source and present a molecular-level model of cell metabolism that explains the dichotomy between copiotrophs-which dominate in carbon-rich environments-and oligotrophs-which dominate in carbon-poor environments-as the consequence of trade-offs between nutrient transport systems. While prototypical copiotrophs, like Vibrios, possess numerous phosphotransferase systems (PTS), prototypical oligotrophs, such as SAR11, lack PTS and rely on ATP-binding cassette (ABC) transporters, which use binding proteins. We develop models of both transport systems and use them in proteome allocation problems to predict the optimal nutrient uptake and metabolic strategy as a function of carbon availability. We derive a Michaelis-Menten approximation of ABC transport, analytically demonstrating how the half-saturation concentration is a function of binding protein abundance. We predict that oligotrophs can attain nanomolar half-saturation concentrations using binding proteins with only micromolar dissociation constants and while closely matching transport and metabolic capacities. However, our model predicts that this requires large periplasms and that the slow diffusion of the binding proteins limits uptake. Thus, binding proteins are critical for oligotrophic survival yet severely constrain growth rates. We propose that this trade-off fundamentally shaped the divergent evolution of oligotrophs and copiotrophs. Author summary Marine bacteria utilize carbon as a building block and an energy source and thus exert an important control on the amount of carbon that is sequestered in the ocean versus respired into the atmosphere. They use a spectrum of strategies to consume carbon: while copiotrophic bacteria dominate in nutrient-rich environments, oligotrophic bacteria dominate in nutrient-poor environments and are typically smaller, nonmotile, and slower growing. Yet the paragon oligotroph SAR11 is the planet's most abundant organism. Despite this, most of our understanding of bacteria derives from research on copiotrophs. Here we use molecular-level models to understand how an oligotroph's physiology enables it to outperform copiotrophs in nutrient-poor but not in nutrient-rich environments. We contrast copiotrophs' prevalent method of sugar transport with oligotrophs' reliance on binding proteins, which trap nutrients in the periplasm. Binding proteins allow cells to attain affinities that are much higher than the transport proteins' intrinsic affinities. However, our model predicts that attaining such high affinities requires large periplasms with high abundances of the slowly diffusing binding proteins, which precludes high growth rates. By quantifying the benefits and costs of binding proteins, we provide a mechanistic explanation for the divergent evolution of oligotrophs and copiotrophs.

Automated summary

Marine bacterial diversity is influenced by metabolic strategies, with copiotrophs and oligotrophs exhibiting trade-offs in nutrient transport systems. Oligotrophs rely on binding proteins for nutrient uptake, achieving high affinities but limiting growth rates due to large periplasms and slow diffusion of binding proteins. This trade-off has shaped the evolution of oligotrophs and copiotrophs, providing insights into their physiological differences in nutrient-rich and nutrient-poor environments.