Symbionts of predatory protists are widespread in the oceans and related to animal pathogens

Protists are major predators of ocean microbial life, with an ancient history of entanglements with prokaryotes, but their delicate cell structures and recalcitrance to culturing hinder exploration of marine symbioses. We report that tiny oceanic protistan predators, specifically choanoflagellates—the closest living unicellular relatives of animals—and uncultivated MAST-3 form symbioses with four bacterial lineages related to animal symbionts. By targeting living phagotrophs on ship expeditions, we recovered genomes from physically associated uncultivated Legionellales and Rickettsiales. The evolutionary trajectories of Marinicoxiellaceae, Cosmosymbacterales, Simplirickettsiaceae, and previously named Gamibacteraceae vary, including host-engagement mechanisms unknown in marine bacteria, horizontally transferred genes that mediate pathogen-microbiome interactions, and nutritional pathways. These symbionts and hosts occur throughout subtropical and tropical oceans. Related bacteria were detected in public data from freshwater, fish, and human samples. Symbiont associations with animal-related protists, alongside relationships to animal pathogens, suggest an unexpectedly long history of shifting associations and possibilities for host expansion as environments change.