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Metagenomic investigation of deep-sea vent tubeworm endosymbionts from MidCayman Rise reveals new insights into metabolism and diversity Julie Reveillaud1,2, Colleen Cavanaugh2,3, Julie Huber2 1INRA/CIRAD, UMR 117 ASTRE, Montpellier, France 2Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA, USA 3 Harvard University, Department of Organismic and Evolutionary Biology, Cambridge, MA 02138, USA Abstract Two species of vestimentiferan tubeworms (Escarpia sp. and Lamellibrachia sp.2) were reported at an area of low-temperature hydrothermal diffuse vent flow at the MidCayman Rise (MCR) in the Caribbean Sea. Here, we used 16S rRNA and ITS gene cloning, together with electron microscopy and a cultivation-independent metagenomic approach to characterize chemosynthetic symbionts in the trophosome tissue of Escarpia and Lamellibrachia at the MCR. 16S rRNA and ITS gene phylogenetic analysis indicated all MCR individuals harbored endosymbionts that were >99% identical, with ITS sequences forming a separate well-supported clade that diverged from those of symbionts of seep and vent vestimentiferans from the Pacific, Gulf of Mexico, and Mediterranean Sea. The metagenomes of the symbionts of two specimens of each tubeworm species were sequenced and two distinct Gammaproteobacteria genomes of more than 4 Mbp assembled. An Average Nucleotide Identity of 86.5% between these genomes, together with distinct 16S sequences, suggest the presence of several MCR endosymbiont phylotypes, with one draft genome shared between one Escarpia and two Lamellibrachia individuals. Genes for sulfur and hydrogen oxidation, nitrate (assimilatory and dissimilatory) reduction, glycolysis and the Krebs cycle, peptide, sugar, and lipid transporters, and both rTCA and CBB carbon fixation cycles were detected in the genomes, highlighting key and shared functions with symbiont metagenomes of Riftia, Tevnia, and Ridgeia from the Pacific. The potential for a second hydrogen oxidation pathway (via a bidirectional hydrogenase), formate dehydrogenation, a catalase, and several additional peptide transporters were found exclusively in the MCR symbionts. Marked gene content and sequence dissimilarity at the rRNA operon and whole genome level between vent and seep endosymbionts studied herein suggest symbionts from the MCR belong to novel tubeworm endosymbiont strains, possibly adapted to H2-rich (19 mM) systems. The present study further adds new evidence that tubeworm endosymbionts can potentially switch from autotrophic to heterotrophic metabolism and suggest their versatile metabolic potential may enable the host to exploit a wide range of environmental conditions.