Abstract
Bacteriophages (phages) are ubiquitous elements in nature, but their ecology and role in animals remains little understood. Sponges represent the oldest known extant animal-microbe symbiosis and are associated with dense and diverse microbial consortia. Here we investigate the tripartite interaction between phages, bacterial symbionts, and the sponge host. We combined imaging and bioinformatics to tackle important questions on who the phage hosts are and what the replication mode and spatial distribution within the animal is. This approach led to the discovery of distinct phage-microbe infection networks in sponge versus seawater microbiomes. A new correlative in situ imaging approach (‘PhageFISH-CLEM‘) localised phages within bacterial symbiont cells, but also within phagocytotically active sponge cells. We postulate that the phagocytosis of free virions by sponge cells modulates phage-bacteria ratios and ultimately controls infection dynamics. Prediction of phage replication strategies indicated a distinct pattern, where lysogeny dominates the sponge microbiome, likely fostered by sponge host-mediated virion clearance, while lysis dominates in seawater. Collectively, this work provides new insights into phage ecology within sponges, highlighting the importance of tripartite animal-phage-bacterium interplay in holobiont functioning. We anticipate that our imaging approach will be instrumental to further understanding of viral distribution and cellular association in animal hosts.
Highlights
Marine animals are constantly exposed to viruses considering average titres of 10 million virions per millilitre of seawater [1]
We recently discovered a novel symbiont phage-encoded protein in sponges (ANKp) that modulates eukaryote–bacterium interaction by altering the eukaryotes’ response to bacteria and which seems to be widespread in eukaryote host associated systems [12]
We predicted the bacterial hosts of marine sponge-derived phages through a combination of prognostic computational approaches via CRISPR-spacer, tRNA and genome homology, as reviewed in Edwards et al [34]
Summary
Marine animals are constantly exposed to viruses considering average titres of 10 million virions per millilitre of seawater [1]. Direct interactions include e.g. phagocytosis of phage virions by eukaryote cells, as reviewed in Van Belleghem et al [4], while indirect interaction occurs via manipulation of the microbiome by the phage or eukaryote In this context, we recently discovered a novel symbiont phage-encoded protein in sponges (ANKp) that modulates eukaryote–bacterium interaction by altering the eukaryotes’ response to bacteria and which seems to be widespread in eukaryote host associated systems [12]. Marine sponges are sessile filter feeders that are massively exposed to planktonic microbes, including viruses, translating to roughly 56 billion virions filtered by a sponge per day [26, 27] Despite such high exposure rates to seawater microorganisms, they contain highly host species-specific microbial [28, 29] and viral [12, 30] communities. Our work uncovers phages as central elements of the microbial ecology within marine sponges
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