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 colonized a niche with distinct geochemical characteristics. To better understand the metabolic potentials and genomic features contributing to host-environment adaptation, we compared genomes of the symbionts of Bathymodiolus manusensis, Arcovestia ivanovi, and Alviniconcha boucheti sampled at PACManus and discuss their environmental adaptive features. We found that B. manusensis and A. ivanovi are colonized by γ-proteobacteria from distinct clades, whereas endosymbionts of B. manusensis feature high intraspecific heterogeneity with differing metabolic potentials. A. boucheti harbored three novel ϵ-proteobacteria symbionts, suggesting potential species-level diversity of snail symbionts . Genome comparisons revealed gene families related to low pH homeostasis, metal resistance, oxidative stress resistance, environmental sensing/responses, and chemotaxis and motility were most abundant in A. ivanovi's symbiont, followed by symbionts of the vent-mouth-dwelling snail A. boucheti, and relatively low in the vent-periphery-dwelling mussel B. manusensis, which is consistent with their environmental adaptation and host-symbiont interactions. Gene families classified to 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 these symbionts may differ in their host-colonization strategy. Comparison of ϵ-symbionts to non-symbionts demonstrated the expanded gene families in symbionts were related to VB12 synthesis, toxin-antitoxin, methylation, and lipopolysaccharide biosynthesis, suggesting these are vital to symbiotic establishment and development in ϵ-proteobacteria. Importance Deep-sea hydrothermal vents are dominated by several invertebrate species. The establishment of symbiosis has long been thought to be the key to successful colonization by these sedentary species in such harsh environments. Yet the relationships between symbiotic bacteria and their hosts, and their role in environment adaptations generally remain unclear. In this paper, we show that the distribution of three host species showed characteristic niche partitioning in the Manus Basin, giving us opportunity to understand how they adapt to their particular habitats. This study also revealed three novel genomes of symbionts from the snails of A. boucheti. Combined with a dataset of other ectosymbiont and free-living bacteria, genome comparisons of the snail endosymbionts pointed to several genetic traits that may have contributed to the lifestyle shift into the epithelial cells in ϵ-proteobacteria. These findings could increase our understanding of invertebrate–endosymbiont in deep-sea ecosystems.

mTORC1 regulates phagosome digestion of symbiotic bacteria for intracellular nutritional symbiosis in a deep-sea mussel

“…The mussel gills had major genes involved in transporting sterols and amino acids (table S3). The symbionts have genes for some compound transporters, such as ATP-binding cassette (ABC) transporters, and for bacterial secretion systems, including type II (table S3), known to export various proteins in an extracellular manner ( 25 ). The genes of factors related to the inhibition of phagosome digestion and other secretion systems, such as type III, IV, and VI secretion systems, were not found in the transcripts of symbionts in B. japonicus .…”

Mosaic environment-driven evolution of the deep-sea mussel Gigantidas platifrons bacterial endosymbiont

“…Symbiotic bacterial DNA was extracted from the mussel gills following the method described by Li et al (2020) [63]. Briefly, the gill tissues were homogenized with PBS buffer, and the tissue debris in the supernatant were removed by sequential filtration through 10-μm, 5-μm, and 3-μm Millipore nitrocellulose membranes.…”

Ancient endosymbiont‐mediated transmission of a selfish gene provides a model for overcoming barriers to gene transfer into animal mitochondrial genomes

“…Although alpha-proteobacteria are more common non-bilaterian endosymbionts, [29] some marine invertebrates harbor Campylobacterota endosymbionts. [112,113] Campylobacterota are generally extremophilic and/or parasitic bacteria with reduced genome sizes that inhabit habitats such as hydrothermal vents where they may form endosymbiotic associations with marine invertebrates. [112] Octocorals are also found in these environments, presenting opportunities for endosymbiosis with Campylobacterota.…”

“…[112] Octocorals are also found in these environments, presenting opportunities for endosymbiosis with Campylobacterota. [113] It is conceivable that octocorals gained mutS7 via bacterial EGT similar to how sponges, scleractinian corals and placozoans likely gained their nuclear-encoded, presumably mitochondria-targeted [11] MSH1 gene from alpha-proteobacterial endosymbionts. [26,29,114] However, given the MutS7 phylogeny presented here (Figure 2) and previously, [8,11,14] we argue that EGT via the lysogenic stage of a giant virus represents the best model for acquisition of mtMutS in octocorals.…”