Untangling interactions between uncultured marine microbes across domains of life through single-cell genomics and timeseries analysis

Microbes of all lifeforms build the foundation of the marine food web and base of the carbon cycle. Diverse unicellular eukaryotes, many uncultivated, occupy key positions in the food web and have evolved complex lifestyles and interact extensively with bacteria in the surface ocean, with major implications for the flow of energy in the ecosystem. Beyond predator-prey relationships, both photosynthetic and phagocytotic protists engage in relationships with other microbes going beyond classical predator-prey interactions, but those remain poorly characterized. We utilized single cell sorting and whole genome sequencing of marine protists to discover bacteria associated with photosynthetic and heterotrophic protists. Putative symbionts from the Alphaproteobacteria and Gammaproteobacteria associated with heterotrophic protists. They resided within choanoflagellates and the MAST-3 lineages, dominant consumers of the most abundant phytoplankton and other microbes. The choanoflagellate and MAST-3 associated Alpha- and Gammaproteobacteria lineages including causative agents of disease in human, possess specialized adaptations in the host environment, including complete Type IV secretion systems. However, their manner of symbioses differs, following distinct trajectories.

The microbes associated with photosynthetic protists were primarily Planctomycetota, Verrucomicrobiota and Bacteroidota. These members of the phycosphere surrounding the phytoplankton cell encoded pili and flagella enabling varying degrees of motility and attachment in line with an extracellular lifestyle. Observations of microbial interactions changing over time indicates that these interactions are severely impacted by changes in environmental conditions, such as warming of surface waters and a decline in nutrient concentrations, especially in stratified summer conditions in the open ocean, through a decline in phytoplankton and subsequent impact on the heterotrophic community.

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