Multicellular group formation as a resource competition strategy for marine bacteria

Abstract

Multicellularity can enhance bacterial resilience and robustness in nature. Traits like access to otherwise inaccessible substrates, increased stress tolerance and predation resistance provide ecological advantages that may scaffold the evolution of multicellular complexity. While multicellularity arises in many ecological contexts, we lack general principles to predict which environments favor these traits. Here, we ask how the physical size of multicellular groups affects their ability to compete for resources, focusing on marine bacteria that degrade organic matter. These bacteria compete for resources ranging from nanoscale dissolved organic matter to millimeter-scale particles. Using a theory of size-dependent fluid encounters, we identify a regime where resource encounters depend on group size. Experiments with the group-forming marine bacteria Vibrio splendidus 12B01 support the prediction that larger groups encounter resources more frequently. However, analysis of per-capita resource allocation reveals a trade-off: group size is inversely related to both the mean and variance of per-capita encounters. Cells in groups obtain fewer resources per cell than single cells, but experience more consistent encounters, sheltering them from large fluctuations in resource acquisition. Stochastic simulations support this tradeoff and predict a broad range of conditions in which consistency enables multicellular groups to out-compete or coexist with single cells. Our findings suggest that group formation is a potentially widespread but overlooked strategy for resource competition in marine heterotrophic bacteria, shaped by biophysical constraints on resource encounters. Significance StatementMulticellular groups are thought to arise in ecological settings where group-level traits confer a fitness advantage. However, linking these evolutionary drivers to specific ecological mechanisms remains a major challenge in understanding the origins of multicellular life. In this study, we draw inspiration from the microscale ecology of marine bacteria that play a key role in the oceans carbon cycle. These bacteria often rely on high local population densities to secrete enough extracellular enzymes to degrade organic matter and access nutrients. By combining experimental measurements with a mathematical theory of encounters and stochastic simulations of competition dynamics, we show that multicellular bacterial groups often out-compete single cells. Our results suggest that the advantage of multicellular groups stems from a tradeoff between the consistency and quantity of resource encounters, arising from purely physical processes. The physics of encounters offers a generic framework that can be leveraged to understand ecological scaffolds of multicellularity.