A Phage Protein Aids Bacterial Symbionts in Eukaryote Immune Evasion

Phages are increasingly recognized as important members of host-associated microbiomes, with a vast genomic diversity. The new frontier is to understand how phages may affect higher order processes, such as in the context of host-microbe interactions. Here, we use marine sponges as a model to investigate the interplay between phages, bacterial symbionts, and eukaryotic hosts. Using viral metagenomics, we find that sponges, although massively filtering seawater, harbor species-specific and even individually unique viral signatures that are taxonomically distinct from other environments. We further discover a symbiont phage-encoded ankyrin-domain-containing protein, which is widely spread in phages of many host-associated contexts including human. We confirm in macrophage infection assays that the ankyrin protein (ANKp) modulates the eukaryotic host immune response against bacteria. We predict that the role of ANKp in nature is to facilitate coexistence in the tripartite interplay between phages, symbionts, and sponges and possibly many other host-microbe associations. [Display omitted] •Sponges, evolutionary basal animals, represent a reservoir of novel viral diversity•Viromes of neighboring sponges are individually unique and species specific•Phages encode ankyrins to aid bacteria in evading the eukaryotic immune system•Such “Ankyphages” are widespread in host-associated environments, including humans Jahn et al. find that sponges, although massively filtering seawater, host individually unique and species-specific viral communities. An abundant sponge bacteriophage encodes ankyrins that, upon bacterial expression, reduce the eukaryotic immune response and phagocytosis of bacteria. This suggests a mechanism of tripartite phage-bacterium-host interplay with the phage fostering host-microbe symbiosis.