Tetrahymena phagocytic vesicles as ecological micro-niches of phage transfer

The microbial communities in natural environments such as soil, pond water, or animal rumens are composed of a diverse mixture of bacteria and protozoa including ciliates or flagellates. In such microbiomes, a major source of bacterial mortality is grazing by phagocytic protists. Many protists are omnivorous heterotrophs, feeding on a range of different bacterial species. Due to this indiscriminate feeding, different bacterial species can assemble together in the same phagocytic vesicles where they can potentially exchange genetic material. Here we show that Tetrahymena thermophila imports and accumulates phage donor and recipient bacterial strains in its phagocytic vesicles and that under laboratory conditions the ingested bacteria remain viable for ≥2 h. Prophages in the ingested bacteria induce immediately after ingestion, and the released phages are concentrated in the phagocytic vesicles of the ciliate. These phages retain their ability to infect phage-susceptible bacterial strains. As a consequence of being confined within the phagosome, the frequency of lysogen formation in these vesicles increases 6-fold as compared with the bulk solution. Collectively, these observations suggest that T. thermophila aids in dissemination of bacteriophages by accumulating susceptible bacteria and phages in their phagocytic vesicles.