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

Abstract

Summary Relationships fueled by sulfide between deep‐sea invertebrates and bacterial symbionts are well known, yet the diverse overlapping factors influencing symbiont specificity are complex. For animals that obtain their symbionts from the environment, both host identity and geographic location can impact the ultimate symbiont partner. Bacterial symbionts were analysed for three co‐occurring species each of Bathymodiolus mussels and vestimentiferan tubeworms, from three deep methane seeps off the west coast of Costa Rica. The bacterial internal transcribed spacer gene was analysed via direct and barcoded amplicon sequencing to reveal fine‐scale symbiont diversity. Each of the three mussel species (B. earlougheri, B. billschneideri and B. nancyschneideri) hosted genetically distinct thiotrophic endosymbionts, despite living nearly side‐by‐side in their habitat, suggesting that host identity is crucial in driving symbiont specificity. The dominant thiotrophic symbiont of co‐occurring tubeworms Escarpia spicata and Lamellibrachia (L. barhami and L. donwalshi), on the other hand, was identical regardless of host species or sample location, suggesting lack of influence by either factor on symbiont selectivity in this group of animals. These findings highlight the specific, yet distinct, influences on the environmental acquisition of symbionts in two foundational invertebrates with similar lifestyles, and provide a rapid, precise method of examining symbiont identities.

Geography, not lifestyle, explains the population structure of free-living and host-associated deep-sea hydrothermal vent snail symbionts

“…Both population structure and gene content analyses suggest that A. hessleri symbionts form subpopulations that segregate by geography more strongly than by lifestyle. These patterns agree with previous studies of non-symbiotic hydrothermal vent microbial communities, which show that microbes are shaped by their local environment [ 60 ], as well as of host-associated A. hessleri symbiont biogeography at the 16S rRNA gene level [ 27 ] and other horizontally transmitted associations from hydrothermal vents, such as bathymodiolin mussels [ 49 , 61 , 62 ] and provannid snails [ 18 ], that have been shown to partner with habitat-specific symbiont strains. These results, therefore, provide further evidence for horizontal transmission in the A. hessleri symbiont system.…”

Metabolic handoffs between multiple symbionts may benefit the deep-sea bathymodioline mussels

“…The key symbionts of bathymodioline mussels include the sulfur-oxidizing Thioglobaceae (gammaproteobacterial order PS1, also known as the SUP05 clade), and the Methyloprofundus (gammaproteobacterial order Methylococcales) methane-oxidizing bacteria. Some bathymodioline mussels, such as Bathymodiolus earlougheri, B. billschneideri and B. nancyschneideri host single-species populations of thiothrophic symbionts [12], whereas Gigantidas childressi and G. platifrons host mainly the methane-oxidizing bacteria [13–15]. Others host both [10, 16].…”

Metabolic handoffs between multiple symbionts may benefit the deep-sea bathymodioline mussels

“…The key symbionts of bathymodioline mussels include the sulfur-oxidizing Thioglobaceae (gammaproteobacterial order PS1, also known as the SUP05 clade), and the Methyloprofundus (gammaproteobacterial order Methylococcales) methane-oxidizing bacteria. Some bathymodioline mussels, such as Bathymodiolus earlougheri , B. billschneideri and B. nancyschneideri host single-species populations of thiotrophic symbionts [ 11 ], whereas Gigantidas childressi and G. platifrons host mainly the methane-oxidizing bacteria [ 12 – 14 ]. Others host both [ 15 ].…”