Endoriftia response to host-associated and free-living life

Mutualism between microbial symbionts and eukaryote hosts is ubiquitous. One of the most exiting mutualisms is the association between a sulfur bacterium, called Candidatus Endoriftia persephone, and its host Riftia pachyptila. These giant tubeworms live in the deep sea at hydrothermal vents in the Pacific Ocean. The tubeworms reproduce through larvae that do not carry the symbionts. They migrate through the seawater and settle at vents. There, the uptake of the symbiont into the host happens in each host generation anew from a pool of free-living symbionts from the environment. The host has no mouth and gut as adult and is nourished by its symbiont, housed in an organ deep inside the host body. The symbionts receive all chemicals necessary for chemoautotrophy (oxygen, sulfide, carbon dioxide), a process where organic carbon is produced in a similar way to photoautotrophy in plants. In return they feed the host. The tubeworms, however, are highly dependent on the environment in which these chemicals fluctuate. How the symbiont reacts to variable concentrations is not known yet. Upon cessation of vent flow, supplies of chemicals stops and the host dies. The symbionts, however survive because they leave the dead host. How they manage is not known yet. Gene expression patterns in the symbiont from live hosts exposed to different chemical concentrations, from dead hosts, and from free-living hosts in the seawater as well as colonizing surfaces will inform about the physiology of the symbiont. Further we plan to investigate whether the symbiont can live heterotrophically, especially under environmental conditions that do not allow chemosynthesis. Therefore, a suite of experiments was carried out in high-pressure aquaria during two research cruises on the research vessel Atlantis with the submersible Alvin to the Pacific Ocean. This proposed study will enhance our understanding on the evolution of this exceptional partnership

Mutualism between microbial symbionts and eukaryote hosts is ubiquitous. One of the most exiting mutualisms is the association between a sulfur bacterium, called Candidatus Endoriftia persephone, and its host the giant tubeworm Riftia pachyptila from deep-sea hydrothermal vents. The host has no mouth and gut as adult and is nourished by its symbiont. The symbionts receive all chemicals necessary for chemoautotrophy (oxygen, sulfide, carbon dioxide) from the host, a process where organic carbon is produced in a similar way to photoautotrophy in plants. To better understand the interplay between partners we sequenced the genome of the host and closed the genome of the symbiont. Interestingly, the genome of the host is characterized by reductive evolution, highly dependent on an obligate symbiotic life style. In contrast, the symbiont thrives associated with the host but also in the environment with a highly versatile autotrophic and heterotrophic gene repertoire. Metagenome sequencing of free-living and host populations revealed that the symbiont strain variations in the host are dominated by one strain and are a subset of that found in the environment. Gene expression studies on the free-living symbiont conducted in high pressure vessels revealed autotrophy and heterotrophy but analyses have yet to be finished due to a research cruise in summer 2023. Most importantly, this cruise allowed us to investigate how the tubeworms colonize vents. Larvae were previously proposed to settle at vents through downwards swimming or sinking. However, for giant tubeworm, it remains unknown from where and how these larvae arrive to settle at a vent as the larvae have never been found in the water column. An untested hypothesis for the mechanism of dispersal is the transit of larvae through the shallow Earth's crust in porous volcanic rocks, channels and small subsurface cavities. Also, the presence of animal life below vents has never been explored. During this cruise we discovered adult and fertile sessile tubeworms and mobile vent fauna of all trophic levels in the Earth's crust. This finding is to our knowledge unprecedented in the deep sea. We can show that deep-sea hydrothermal vents do not only exist above the seafloor but extend into the subsurface beneath the seafloor.