Genome assembly of the chemosynthetic endosymbiont of the hydrothermal vent snail Alviniconcha adamantis from the Mariana Arc

Abstract

Chemosynthetic animal-microbe symbioses sustain hydrothermal vent communities in the global deep sea. In the Indo-Pacific Ocean, hydrothermal ecosystems are often dominated by gastropod species of the genus Alviniconcha, which live in association with chemosynthetic Gammaproteobacteria or Campylobacteria. While the symbiont genomes of most extant Alviniconcha species have been sequenced, no genome information is currently available for the gammaproteobacterial endosymbiont of Alviniconcha adamantis-a comparatively shallow living species that is thought to be the ancestor to all other present Alviniconcha lineages. Here, we report the first genome sequence for the symbiont of A. adamantis from the Chamorro Seamount at the Mariana Arc. Our phylogenomic analyses show that the A. adamantis symbiont is most closely related to Chromatiaceae endosymbionts of the hydrothermal vent snails Alviniconcha strummeri and Chrysomallon squamiferum, but represents a distinct bacterial species or possibly genus. Overall, the functional capacity of the A. adamantis symbiont appeared to be similar to other chemosynthetic Gammaproteobacteria, though several flagella and chemotaxis genes were detected, which are absent in other gammaproteobacterial Alviniconcha symbionts. These differences might suggest potential contrasts in symbiont transmission dynamics, host recognition, or nutrient transfer. Furthermore, an abundance of genes for ammonia transport and urea usage could indicate adaptations to the oligotrophic waters of the Mariana region, possibly via recycling of host- and environment-derived nitrogenous waste products. This genome assembly adds to the growing genomic resources for chemosynthetic bacteria from hydrothermal vents and will be valuable for future comparative genomic analyses assessing gene content evolution in relation to environment and symbiotic lifestyles.

Keywords: Alviniconcha adamantis; Mariana Arc; chemosynthetic symbiosis; hydrothermal vents.

Fig. 1.

Sampling location of Alviniconcha adamantis in the Mariana Arc, from which the symbiont genome reported here was isolated. Habitats of other host species with closely related symbionts are shown, A. strummeri in the Lau Basin and Chrysomallon squamiferum on the Central Indian Ridge. The map was produced with the marmap package (Pante and Simon-Bouhet, 2013) in R.

Fig. 2.

a) Representative phylogeny of chemosynthetic Gammaproteobacteria, for which whole-genome sequences were available (Supplementary Table 2). The A. adamantis symbiont forms a sister clade to the Chromatiaceae symbionts of A. strummeri and C. squamiferum despite the vast geographic distances among the habitats of these species. Numbers on nodes indicate support values from ultrafast bootstrapping and Shimodaira–Hasegawa-like approximate likelihood ratio tests. b) Pangenome of the A. adamantis, A. strummeri, and C. squamiferum symbionts. Symbiont contigs are shown as purple layers, while number of genes and combined homogeneity indices of gene clusters are shown as blue layers. The homogeneity index is a measure of amino acid sequence similarity within computed gene clusters, with higher values indicating more homogeneous clusters. The 3 symbionts share 1,325 core protein-coding gene clusters (containing 4,167 genes), while approximately the same amount of gene clusters is exclusive to the A. adamantis symbiont in agreement with the genomic and phylogenetic divergence among symbiont species. The matrix on the right shows average nucleotide identities among symbiont genomes from 70% to 100%, with darker grey tones indicating higher identities.

Fig. 3.

Completeness of KEGG metabolic pathways in the A. adamantis symbiont compared to its closest bacterial relatives (left) and functional similarity to other chemosynthetic Gammaproteobacteria (right). In contrast to phylogenetic proximity, the A. adamantis and C. squamiferum symbionts are more similar to each other in terms of functional potential than either of these species to the A. strummeri symbiont.