Prochlorococcus extracellular vesicles: molecular composition and adsorption to diverse microbes

Extracellular vesicles are small (50-200 nm diameter) membrane-bound structures released by cells from all domains of life. Vesicles have been implicated in numerous microbial processes, including gene transfer, signaling, pathogenesis, and defense. While vesicles are abundant in the oceans, little is known about their contents or whether they interact with cells in this dilute environment. Here we show that extracellular vesicles contain a remarkable diversity of organic carbon compounds and likely mediate a complex network of export, transport and exchange within marine microbial communities. We report that vesicles from selected strains of Prochlorococcus, the most abundant cyanobacterium in the sea, and other bacteria can interact with cells of various marine microbes, including the numerically abundant heterotroph Pelagibacter. Through a combination of lipidomic, metabolomic and proteomic analyses, we show that two strains of Prochlorococcus export an enormous array of organic and inorganic compounds – including active, biogeochemically relevant enzymes – within vesicles. Vesicles from both strains contained some materials in common as well as numerous strain-specific differences, reflecting an even greater degree of functional complexity within natural vesicle populations. These data suggest additional roles for vesicles in carrying out extracellular biogeochemical reactions, mitigating toxicity from reactive oxygen species, and mediating energy and nutrient transfers in the oceans.