Physical Proximity May Promote Lateral Acquisition of Bacterial Symbionts in Vesicomyid Clams

Abstract

Vesicomyid clams harbor intracellular sulfur-oxidizing bacteria that are predominantly maternally inherited and co-speciate with their hosts. Genome recombination and the occurrence of non-parental strains were recently demonstrated in symbionts. However, mechanisms favoring such events remain to be identified. In this study, we investigated symbionts in two phylogenetically distant vesicomyid species, Christineconcha regab and Laubiericoncha chuni, which sometimes co-occur at a cold-seep site in the Gulf of Guinea. We showed that each of the two species harbored a single dominant bacterial symbiont strain. However, for both vesicomyid species, the symbiont from the other species was occasionally detected in the gills using fluorescence in situ hybridization and gene sequences analyses based on six symbiont marker genes. Symbiont strains co-occurred within a single host only at sites where both host species were found; whereas one single symbiont strain was detected in C. regab specimens from a site where no L. chuni individuals had been observed. These results suggest that physical proximity favored the acquisition of non-parental symbiont strains in Vesicomyidae. Over evolutionary time, this could potentially lead to genetic exchanges among symbiont species and eventually symbiont displacement. Symbiont densities estimated using 3D fluorescence in situ hybridization varied among host species and sites, suggesting flexibility in the association despite the fact that a similar type of metabolism is expected in all symbionts.

Phylogeny and origins of chemosynthetic vesicomyid clams

“…These chemoautotrophic, sulphur-oxidizing gammaproteobacteria provide most or all of the clams' nutrition (Dubilier, Bergin, & Lott, 2008;Felbeck, 1981;Fisher et al, 1988). The symbionts are transmitted vertically to the next generation via the clams' eggs (Cary, Warren, Anderson, & Giovannoni, 1993;Endow & Ohta, 1990;Hurtado, Mateos, Lutz, & Vrijenhoek, 2003;Szafranski, Gaudron, & Duperron, 2014), notwithstanding that separate cases of lateral acquisition have been reported (Decker, Olu, Arnaud-Haond, & Duperron, 2013;Stewart, Young, Cavanaugh, 2008). This symbiotic relationship has resulted in a pattern of co-speciation between the host and symbiont phylogenies (Distel, Felbeck, & Cavanaugh, 1994;Peek, Feldman, Lutz, & Vrijenhoek, 1998).…”

An overview of chemosynthetic symbioses in bivalves from the North Atlantic and Mediterranean Sea

“…In Vesicomyidae, lateral acquisition of non-parental symbiont strains, probably promoted by physical closeness, has been documented in several species (Fig. 4b, Stewart et al, 2008;Decker et al, 2013).…”

“…Several species can co-occur at a given seep or vent site, sometimes within a single clam aggregate, as observed in the Gulf of Guinea with Christineconcha regab and Laubiericoncha chuni Krylova and Cosel, 2011). Physiological differences between some species could account for slight ecological niche differentiation and prevent competition (Goffredi and Barry, 2002;Decker at al., 2013).…”

“…Host and symbiont phylogenies can be superimposed, suggesting rather strict co-speciation (Peek et al, 1998a, b). However, a limited amount of lateral transfer does exist and may permit gene exchanges between symbiont lineages (Stewart et al, 2008(Stewart et al, , 2009bDecker et al, 2013). To date, the Vesicomyidae are the only deepsea chemosymbiotic metazoans for which symbiont genomes are fully sequenced -namely Candidatus "Vesicomyosocius okutanii" and Candidatus "Ruthia magnifica", in two species from the Pacific (Kuwahara et al, 2007;Newton et al, 2007).…”

“…The genus Isorropodon consists of various species colonizing a wide range of depths (150-6800 m), and could represent a suitable case study into the barriers influencing the biogeography and evolution of vesicomyid symbioses, as demonstrated by the recent discovery of I. perplexum in the Sea of Marmara (Ritt et al, 2012). Finding closely related symbionts in closely related species is somewhat expected, although instances of non-parental acquisition are reported (Stewart et al, 2008(Stewart et al, , 2009bDecker et al, 2013). The homogeneity of symbiont populations within a single species was also questioned recently by the finding of distinct bacterial 16S rRNA lineages in distinct specimens of Calyptogena valdiviae (Fig.…”