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

Background In deep-sea hydrothermal vents ecosystems, most animals harbor symbiotic communities supporting their nutrition. This is the case of both shrimps 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, the second in the foregut and the last one in the midgut, 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 structuration in the holobiont remain unknown. We combined Fluorescent in situ Hybridization, metabarcoding and genome-resolved metagenomics data to reveal a part of their evolution, contribution to the holobiont functioning and their metabolic potential. For this, 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 digestive Lachnospirales family in the midgut. This novel symbiont showed the capacity to degrade host’s chitin, to fix carbon dioxide thanks to secondary pathways, to use oxygen and to encode for flagellar genes implied in host-symbiont recognition. In addition, they harbor CRISPR/cas genes that may be involved in the holobiont defense. Lachnospirales seemed to colonize the ectoperitrophic space, were submitted to elongation without dividing themselves and are acquired post-installation of the juveniles on active sites. Consequently, they share many commonalities with Candidatus Microvillispirillaceae, which they co-occur with. Conclusion Our data suggest that the Lachnospirales would be mixotrophic and would live in syntrophy with Candidatus Microvillispirillaceae. Indeed, they could degrade chitin, allowing Ca. Microvillispirillaceae to use degradation products for their metabolism. As Ca. Microvillispirillaceae, they are acquired post-installation during metamorphosis. Consequently, both symbionts may strongly contribute to the holobiont fitness.