Phages associated with animal holobionts in deep-sea hydrothermal vents and cold seeps

Deep-sea environments are harsh habitats; however, many animal taxa flourish in deep-sea ecosystems such as vents and seeps. The success of those animals in such habitats has been attributed to their symbiotic relationships with diverse microorganisms. Previous studies extensively examined the roles of chemoautotrophic bacteria in symbiotic systems, revealing that they are essential to the ecological adaptation of animal holobionts. Some recent studies have focused on the influence of viral partners on the bacterial symbionts in deep-sea animals, which shows that bacterial viruses (bacteriophages/phages) might also play important roles in the deep ocean symbiosis. In the present review, we deduce phage-bacteria interactions from existing literature, newer comparative analyses, and considerations of microbial adaptation to extreme environments. In the analyses, we specifically investigated viral signals in hologenomes of animals in hydrothermal vents and cold seeps and discussed the potential roles of phages in symbiosis maintenance. Metagenome investigation reveals diverse phage families in the holobionts of mussels, clams, sponges, tubeworms, and snails. Phages in symbiotic systems of vents and seeps may undergo a lysogenic life cycle. The metabolic genes in phage genomes can complement or compensate bacterial symbiont metabolism. In seep mussels and tubeworms, the presence of phage-born immunity-related genes may aid bacterial symbionts in immune evasion by reducing animal phagocytosis. Furthermore, lysis by phages may mediate nutritional supply to deep-sea animals by lysing bacterial cells. For the sponges with relatively high microbial diversity, the diversity may be sustained through phage infection of dominant bacterial symbionts, thereby contributing to animal fitness. We propose a mutualistic tripartite symbiosis model to illustrate the relationships of phages, bacteria, and animals in deep-sea vent/seep ecosystems.

Automated summary

Deep-sea animals in symbiotic relationships with bacteria may also interact with bacterial viruses (bacteriophages) which play important roles in their adaptation and immune evasion. The viruses can complement or compensate for bacterial symbiont metabolism and supply nutrients to deep-sea animals through lysing bacterial cells. This mutualistic tripartite symbiosis model illustrates the relationships between phages, bacteria, and animals in deep-sea vent/seep ecosystems.