Abstract Deep-sea hydrothermal vent ecosystems are sustained by chemoautotrophic bacteria that symbiotically provide organic matter to their animal hosts through the oxidation of chemical reductants in vent fluids. Hydrothermal vents also support unique viral communities that often exhibit high host-specificity and frequently integrate into host genomes as prophages; however, little is known about the role of viruses in influencing the chemosynthetic symbionts of vent foundation fauna. Here, we present a comprehensive examination of contemporary lysogenic and lytic bacteriophage infections, auxiliary metabolic genes (AMGs), and CRISPR spacers associated with the intracellular bacterial endosymbionts of snails and mussels at hydrothermal vents in the Lau Basin (Tonga). Our investigation of contemporary phage infection among bacterial symbiont species and across distant vent locations indicated that each symbiont species interacts with different phage species across a large geographic range. Surprisingly, prophages were absent from almost all symbiont genomes, suggesting that phage interactions with intracellular symbionts may differ from free-living microbes at vents. Altogether, these findings suggest that chemosynthetic symbionts primarily interact with species-specific phages via lytic infections, which may ultimately be important to the composition and dynamics of symbiont populations.
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Horizontal transmission enables flexible associations with locally adapted symbiont strains in deep-sea hydrothermal vent symbioses
Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria , this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species-level associations and influences genetic structuring, connectivity, and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across an ∼800-km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Symbiont strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor widespread genetic connectivity and ecological resilience unless physical dispersal barriers are present.
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- PAR ID:
- 10349121
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 119
- Issue:
- 14
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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