The Marine Cyanobacterium Prochlorococcus Releases Diverse ‘Dissolved’ Organic Molecules Within Extracellular Vesicles

Extracellular vesicles are small (~100 nm diameter) membrane-bound structures released by cells from all domains of life and which are abundant in the oceans. The functional roles of vesicles within marine systems are not known, though they have been implicated in diverse microbial processes including facilitating interactions and chemical exchanges between cells and their environment. Vesicles are a component of marine DOM, capable of containing diverse types of secreted organic compounds including lipids, proteins, nucleic acids, and small molecules. To expand our understanding of the chemical composition of marine extracellular vesicles, we conducted a detailed set of lipidomic, proteomic and metabolomic analyses of vesicles produced by two strains of the most abundant cyanobacterium in the ocean, Prochlorococcus. We found that Prochlorococcus exports an enormous array of compounds within vesicles, including thousands of polar and non-polar mass features. We identified hundreds of proteins within Prochlorococcus extracellular vesicle populations, including functional enzymes that can act on components of marine DOM. Vesicles from two significantly different Prochlorococcus strains contained some materials in common as well as numerous strain-specific differences, reflecting functional complexity within natural vesicle populations. We also found that vesicles from Prochlorococcus and multiple heterotrophic bacteria can interact with other marine microbes, including the numerically abundant Pelagibacter. These results demonstrate that microbial contributions to marine DOM pools can come both in the form of truly ‘dissolved’ individual molecules as well as in the context of locally structured, colloidal vesicles, which may have distinct accessibility and stability in the ocean.