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Parallel Evolution of Key Genomic Features and Cellular Bioenergetics Across the Marine Radiation of a Bacterial Phylum

Diverse bacterial and archaeal lineages drive biogeochemical cycles in the global ocean, but the evolutionary processes that have shaped their genomic properties and physiological capabilities remain obscure. Here we track the genome evolution of the globally-abundant marine bacterial phylum Marinimicrobia across its diversification into modern marine environments and demonstrate that extant lineages have repeatedly switched between epipelagic and mesopelagic habitats. Moreover, we show that these habitat transitions have been accompanied by repeated and fundamental shifts in genomic organization, cellular bioenergetics, and metabolic modalities. Lineages present in epipelagic niches independently acquired genes necessary for phototrophy and environmental stress mitigation, and their genomes convergently evolved key features associated with genome streamlining. Conversely, lineages residing in mesopelagic waters independently acquired nitrate respiratory machinery and a variety of cytochromes, consistent with the use of alternative terminal electron acceptors in oxygen minimum zones (OMZs). Further, while surface water clades have retained an ancestral Na+-pumping respiratory complex, deep water lineages have largely replaced this complex with a canonical H+-pumping respiratory complex I, potentially due to the increased efficiency of the latter together with more energy-limiting environments deep in the ocean’s interior. These parallel evolutionary trends across disparate clades suggest that the evolution of key features of genomic organization and cellular bioenergetics in abundant marine lineages may in some ways be predictable and driven largely by environmental conditions and nutrient dynamics.