A novel digestive symbiont for both holobiont Rimicaris exoculata and Rimicaris chacei: the case of Lachnospirales

Abstract Background In deep-sea hydrothermal vent ecosystems, most animals harbor symbiotic communities that support their nutrition. This is the case for the shrimp Rimicaris exoculata and Rimicaris chacei , two endemic species of the Mid-Atlantic Ridge (MAR), housing three distinct bacterial symbiotic communities playing a major role in their nutrition and scaling up their immune systems. One is located in the cephalothoracic cavity, another in the foregut and the third in the midgut that is mostly represented by Candidatus Microvillispirillaceae. However, recent metabarcoding and metagenomics studies reported for the first time the presence of another abundant potential digestive symbiont representing a novel family of Lachnospirales . To date, their role and organization in the holobiont remain unknown. We combined Fluorescent in situ Hybridization, metabarcoding and genome-resolved metagenomics data to investigate their contribution to the holobiont functioning and their metabolic potential. For this purpose, we used the raw reads of a recent metabarcoding analysis and Metagenome-Assembled Genomes (MAGs) obtained in a previous study. Results We studied two MAGs reconstructed from TAG and Snake Pit sites (MAR) revealing a novel midgut-associated Lachnospirales family. This novel symbiont shows the capacity to degrade host chitin, utilize oxygen and encode flagellar genes involved in host-symbiont recognition. In addition, this Lachnospirales family harbors CRISPR/cas genes that may contribute to the holobiont’s defense. This symbiotic lineage seems to colonize the ectoperitrophic space, undergo elongation without dividing and may be acquired after juvenile settlement at active vent sites. Consequently, they share many commonalities with Candidatus Microvillispirillaceae, with which they co-occur. Conclusion Our data suggest that the Lachnospirales may engage in a syntrophic relationship with Candidatus Microvillispirillaceae. They may be able to degrade chitin, allowing Ca. Microvillispirillaceae to use degradation products for their metabolism. Like Ca. Microvillispirillaceae, Lachnospirales are acquired post-installation of juveniles between stage B and subadult metamorphosis. Consequently, both symbionts may strongly contribute to the holobiont fitness.