Ancient Occasional Host Switching of Maternally Transmitted Bacterial Symbionts of Chemosynthetic Vesicomyid Clams

Abstract

Vesicomyid clams in deep-sea chemosynthetic ecosystems harbor sulfur-oxidizing bacteria in their gill epithelial cells. These symbionts, which are vertically transmitted, are species-specific and thought to have cospeciated with their hosts. However, recent studies indicate incongruent phylogenies between some vesicomyid clams and their symbionts, suggesting that symbionts are horizontally transmitted. To more precisely understand the evolution of vesicomyid clams and their symbionts, we compared the evolution of vesicomyid clams and their symbionts through phylogenetic analyses using multi-gene data sets. Many clades in the phylogenetic trees of 13 host species (Abyssogena mariana, Ab. phaseoliformis, Akebiconcha kawamurai, Calyptogena fausta, C. laubieri, C. magnifica, C. nautilei, C. pacifica, Isorropodon fossajaponicum, Phreagena kilmeri, Ph. okutanii, Ph. soyoae, and Pliocardia stearnsii) and their symbionts were well resolved. Six of the 13 host-symbiont pairs (C. fausta, C. magnifica, C. pacifica, Ph. kilmeri, Ph. okutanii, and Ph. soyoae, and their respective symbionts) showed topological congruence. However, the remaining seven pairs (Ak. kawamurai, Ab mariana, Ab. phaseoliformis, C. laubieri, C. nautilei, I. fossajaponicum, and Pl. stearnsii and their corresponding symbionts) showed incongruent topologies, which were supported by the approximately unbiased and Bayes factor tests. Coevolution analyses indicated that six pairs cospeciated, whereas host switching events occurred in the remaining seven pairs. Markedly, multiple host switching events may have occurred in the lineages from the common ancestral symbiont of C. pacifica and C. fausta. Our phylogenetic and coevolution analyses provide additional evidence for host switching during the evolution of vesicomyids.

Keywords: cospeciation; endosymbiosis; host switching; phylogenetic tree; vertical transmission.

Fig. 1.

—Comparison of Maximum Likelihood (ML) phylogenies for 13 species of vesicomyid clams and their symbionts. (A) ML tree of vesicomyid clams based on the concatenated data sets of nucleotide sequences of 11 mitochondrial genes (atp6, atp8, cox1, cox2, cox3, cob, nad1, nad3, nad4, nad5, and rrnL). Venerid species (Meretrix lusoria, M. meretrix, M. petechialis, Paphia euglypta, and Venerupis philippinarum) were used as outgroups. (B) ML phylogenetic tree of 13 vesicomyid symbionts based on concatenated data sets of the nucleotide sequences of eight genes (16S rRNA, 23S rRNA, galU, groEL, groES, mfd, uvrA, and uvrD paralog). The symbiont of Bathymodiolus septemdierum was used as an outgroup. Dotted lines between vesicomyid clam species and their symbionts’ trees indicate symbiotic pairs. Numbers at the bipartitions indicate ML bootstrap supports of < 100% (left) and Bayesian posterior probabilities of < 1.0 (right). Unlabeled nodes are fully supported (100% bootstrap support and posterior probability at 1.0). Small letters in the squares of some nodes indicate the monophyletic clades described in the text. The orange branches are those exhibiting incongruence between the topologies of the host clams and symbionts, as indicated by an approximately unbiased (AU) test (P < 0.05) and Bayes factor test (>5). Host and symbiont trees were not drawn to the same rate scale, and scale bars indicate the rate of internal nodes except for outgroups.

Fig. 2.

—Coevolution scenarios between the vesicomyid clams and their symbionts. The coevolution analysis was performed using two reconciliation methods, the Jane 4.0 and CoRe-PA. Two preferred coevolutionary patterns exhibiting minimal total cost were selected, (A) Jane 4.0 and CoRe-PA, and (B) Jane 4.0. The black and orange topologies indicate the topologies of the hosts and symbionts, respectively, and the black and orange numbers at the bipartitions indicate the ML bootstrap supports of < 100% (left) and Bayesian posterior probabilities of < 1.0 (right) on host and symbiont trees, respectively. Unlabeled nodes are fully supported (100% bootstrap support and posterior probability of 1.0). The numbers in the orange open circles and small letters in the orange closed circles indicate cospeciation and host switching events, respectively.