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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.