Metagenomic analysis suggests broad metabolic potential in extracellular symbionts of the bivalve Thyasira cf. gouldi

Abstract

Background: Next-generation sequencing has opened new avenues for studying metabolic capabilities of bacteria that cannot be cultured. Here, we provide a metagenomic description of chemoautotrophic gammaproteobacterial symbionts associated with Thyasira cf. gouldi, a sediment-dwelling bivalve from the family Thyasiridae. Thyasirid symbionts differ from those of other bivalves by being extracellular, and recent work suggests that they are capable of living freely in the environment. Results: Thyasira cf. gouldi symbionts appear to form mixed, non-clonal populations in the host, show no signs of genomic reduction and contain many genes that would only be useful outside the host, including flagellar and chemotaxis genes. The thyasirid symbionts may be capable of sulfur oxidation via both the sulfur oxidation and reverse dissimilatory sulfate reduction pathways, as observed in other bivalve symbionts. In addition, genes for hydrogen oxidation and dissimilatory nitrate reduction were found, suggesting varied metabolic capabilities under a range of redox conditions. The genes of the tricarboxylic acid cycle are also present, along with membrane bound sugar importer channels, suggesting that the bacteria may be mixotrophic. Conclusions: In this study, we have generated the first thyasirid symbiont genomic resources. In Thyasira cf. gouldi, symbiont populations appear non-clonal and encode genes for a plethora of metabolic capabilities; future work should examine whether symbiont heterogeneity and metabolic breadth, which have been shown in some intracellular chemosymbionts, are signatures of extracellular chemosymbionts in bivalves.

The Symbiotic “All-Rounders”: Partnerships between Marine Animals and Chemosynthetic Nitrogen-Fixing Bacteria

“…Symbiont-hosting and symbiont-free individuals of one particular thyasirid species are found cooccurring in nature, which shows that this association is likely an optional nutritional supplement, rather than essential for survival ( 4 – 6 ). The symbionts have estimated genome sizes typical of their closest free-living relatives and can probably survive in a free-living form in the environment ( 7 ). Most chemosynthetic symbioses are horizontally transmitted, meaning they are acquired from the environment or from cooccurring hosts during development ( 8 ).…”

Host–Symbiont Interactions in Deep-Sea Chemosymbiotic Vesicomyid Clams: Insights From Transcriptome Sequencing

“…Endosymbionts housed in deep-sea mussels and tubeworms have a transport system to take up various carbohydrates (Robidart et al, 2008;Ho et al, 2017;McCuaig et al, 2018). On the contrary, the endosymbionts of the deep-sea vesicomyid clams reportedly lacked the genes related to the systems for absorbing phosphoenolpyruvate-dependent sugar in the genomes (Kuwahara et al, 2007).…”

Reduced chemosymbiont genome in the methane seep thyasirid and the cooperated metabolisms in the holobiont under anaerobic sediment

“…Thyasira cf. gouldii symbiont is observed as type 2, which is classified into the genus Sedimenticola (family Sedimenticolaceae) based on 16S rRNA gene sequence (McCuaig et al, 2020). The newly released output about C. bisecta clearly demonstrated that these symbionts were aggregated in the apical vesicles (type 3) and might have pathways connecting to environment (Guo et al, 2023), which is consistent with the earlier identification (a more advanced state) by Dufour (2005).…”

“…Thyasira cf. gouldii and Conchocele bisecta ) with the metabolic potentials of the host/symbiont have been studied using the metagenomic approach (Guo et al, 2023; McCuaig et al, 2020). There are only 15 bacterial 16S rRNA gene sequences from the potential thyasirid symbionts on GenBank (last access Jan 2023) and one metagenome‐assembled genome of C. bisecta symbiont (Guo et al, 2023).…”