Evolution of hunt, kill, devour in a Vibrio ecospecies

Abstract

Understanding the molecular and evolutionary basis of adaptation is a central challenge in biology. We have recently identified bacterial "ecospecies": strains that share a well-mixed gene pool with the rest of the species in most of the genome, but carry nearly fixed differences in [~]100 coadapted genes. We hypothesized this structure reflects ecological selection, but ecospecies have so far been characterized only genomically. Here, using "Molassodon" of the marine bacterium Vibrio parahaemolyticus, we provide first experimental evidence linking a multilocus ecospecies genotype to a laboratory phenotype. We find that Molassodon swimming in viscous environments is enhanced by differentiated lateral flagella that no longer drive surface swarming. Using Tn-seq, RNA-seq, and molecular genetics, we link differentiated Type VI secretion and nutrient uptake genes to the swimming phenotype, potentially invoking a natural adaptation related to "hunting". We also identify a convergent genotype also linking lateral flagella and nutrient uptake, suggesting ecological differentiation in V. parahaemolyticus occurs along recurring phenotypic axes and involves borrowing traits from a broader Vibrio gene pool. Together, our results provide first experimental evidence that ecospecies are functionally coherent units and illustrate how they can provide a window into the complex adaptations that shape bacterial ecology.