High‐contiguity genome assembly of the chemosynthetic gammaproteobacterial endosymbiont of the cold seep tubeworm Lamellibrachia barhami

Abstract

Symbiotic relationships between vestimentiferan tubeworms and chemosynthetic Gammaproteobacteria build the foundations of many hydrothermal vent and hydrocarbon seep ecosystems in the deep sea. The association between the vent tubeworm Riftia pachyptila and its endosymbiont Candidatus Endoriftia persephone has become a model system for symbiosis research in deep‐sea vestimentiferans, while markedly fewer studies have investigated symbiotic relationships in other tubeworm species, especially at cold seeps. Here we sequenced the endosymbiont genome of the tubeworm Lamellibrachia barhami from a cold seep in the Gulf of California, using short‐ and long‐read sequencing technologies in combination with Hi‐C and Dovetail Chicago libraries. Our final assembly had a size of ~4.17 MB, a GC content of 54.54%, 137X coverage, 4153 coding sequences, and a CheckM completeness score of 97.19%. A single scaffold contained 99.51% of the genome. Comparative genomic analyses indicated that the L. barhami symbiont shares a set of core genes and many metabolic pathways with other vestimentiferan symbionts, while containing 433 unique gene clusters that comprised a variety of transposases, defence‐related genes and a lineage‐specific CRISPR/Cas3 system. This assembly represents the most contiguous tubeworm symbiont genome resource to date and will be particularly valuable for future comparative genomic studies investigating structural genome evolution, physiological adaptations and host‐symbiont communication in chemosynthetic animal‐microbe symbioses.

Contrasting influences on bacterial symbiont specificity by co‐occurring deep‐sea mussels and tubeworms

“…In addition to habitat type, water depth (and the associated physical parameters such as pressure, temperature, density) has been proposed to structure the surrounding free‐living bacterial populations available for symbiont infection (McMullin et al ., 2003; Thiel et al ., 2012; Zimmermann et al ., 2014). More recent studies have suggested that individual vestimentiferans can host multiple 16S rRNA symbiont phylotypes (Duperron et al ., 2009; Zimmermann et al ., 2014; Patra et al ., 2016) and by using variable genetic markers, such as the symbiont ITS gene, metagenomic studies, and DNA fingerprinting of different vestimentiferan host species, we now know of much greater intra‐host diversity beyond the 16S rRNA gene marker level (Di Meo et al ., 2000; Vrijenhoek et al ., 2007; Harmer et al ., 2008; Reveillaud et al ., 2018; Polzin et al ., 2019; Breusing et al ., 2020b). With the discovery of greater intra‐host symbiont variation in vestimentiferan tubeworms, the influence of the environment on symbiont composition and diversity at local levels offers an interesting point of comparison to co‐occurring Bathymodiolus mussels in the current study.…”

The worm affair: fidelity and environmental adaptation in symbiont species that co‐occur in vestimentiferan tubeworms

“…Read mapping confirmed that this was not a binning artefact, and some remnants of the Nap gene cluster were found in Palmahim B MAGs ( napC and partial napB ). The respiratory nitrate reductase Nar, which sporadically occurs in tubeworm symbionts (Breusing et al ., 2020b), was found only in the genomes Eratosthenes and Palmahim symbionts (both A and B, narQKGHIJ ). Bacteria use the high‐affinity Nap under nitrate limitation, while Nar, which is more favourable for ATP synthesis, is upregulated at high (mM) nitrate concentrations (Moreno‐Vivián et al ., 1999; Kraft et al ., 2011).…”

The complete and closed genome of the facultative generalist Candidatus Endoriftia persephone from deep‐sea hydrothermal vents

“…The percentage of uncharacterised predicted genes (i.e., genes with either unknown function or that remain unannotated) in Endoriftia genome (797 genes/25% of the total) and in the most complete genome of cold-seep endosymbiont available to date (endosymbiont of Lamellibrachia barhami; 1239/27%) (Breusing et al, 2020) is similar. This indicates that the function of a large number of genes in the tubeworm's endosymbiont genomes remains unknown.…”