Endosymbionts of Metazoans Dwelling in the PACManus Hydrothermal Vent: Diversity and Potential Adaptive Features Revealed by Genome Analysis

Abstract

Deep-sea hydrothermal vent communities are dominated by invertebrates, namely, bathymodiolin mussels, siboglinid tubeworms, and provannid snails. Symbiosis is considered key to successful colonization by these sedentary species in such extreme environments. In the PACManus vent fields, snails, tubeworms, and mussels each colo-nized a niche with distinct geochemical characteristics. To better understand the meta-bolic potentials and genomic features contributing to host-environment adaptation, we compared the genomes of the symbionts of Bathymodiolus manusensis, Arcovestia ivanovi, and Alviniconcha boucheti sampled at PACManus, and we discuss their environ-mentally adaptive features. We found that B. manusensis and A. ivanovi are colonized by Gammaproteobacteria from distinct clades, whereas endosymbionts of B. manusensis fea-ture high intraspecific heterogeneity with differing metabolic potentials. A. boucheti har-bored three novel Epsilonproteobacteria symbionts, suggesting potential species-level di-versity of snail symbionts. Genome comparisons revealed that the relative abundance of gene families related to low-pH homeostasis, metal resistance, oxidative stress resistance, environmental sensing/responses, and chemotaxis and motility was the highest in A. ivanovi’s symbiont, followed by symbionts of the vent-mouth-dwelling snail A. boucheti, and was relatively low in the symbiont of the vent-periphery-dwelling mussel B. manusensis, which is consistent with their environmental adaptations and host-symbiont interactions. Gene families classified as encoding host interaction/attachment, virulence factors/toxins, and eukaryotic-like proteins were most abundant in symbionts of mussels and least abundant in those of snails, indicating that these symbionts may differ in their host colonization strategies. Comparison of Epsilonproteobacteria symbionts to nonsym-bionts demonstrated that the expanded gene families in symbionts were related to vita-min B12 synthesis, toxin-antitoxin systems, methylation, and lipopolysaccharide biosyn-thesis, suggesting that these are vital to symbiont establishment and development in Epsilonproteobacteria.