Lateral symbiont acquisition in a maternally transmitted chemosynthetic clam endosymbiosis

Deep-sea clams of the family Vesicomyidae live in symbiosis with intracellular chemosynthetic bacteria. These symbionts are transmitted maternally (vertically) between host generations and should therefore show a pattern of genetic variation paralleling that of the cotransmitted host mitochondrion. However, instances of lateral (nonvertical) symbiont acquisition could still occur, thereby decoupling symbiont and mitochondrial phylogenies. Here, we provide the first evidence against strict maternal cotransmission of symbiont and mitochondrial genomes in vesicomyids. Analysis of Vesicomya sp. mt-II clams from hydrothermal vents on the Juan de Fuca Ridge (northeastern Pacific) revealed a symbiont phylotype (designated symB(VII)) highly divergent from previously described symbionts of the same host lineage. SymB(VII)-hosting clams occurred at low frequency (0.02) relative to individuals hosting the dominant symbiont phylotype. Phylogenetic analysis of 16S rRNA genes from a wide range of symbionts and free-living bacteria clustered symB(VII) within the monophyletic clade of vesicomyid symbionts. Further analysis of 3 symbiont loci (23S, dnaK, and soxA) across 11 vesicomyid taxa unambiguously placed symB(VII) as sister to the symbiont of a distantly related host lineage, Vesicomya sp. from the Mid-Atlantic Ridge (98.9% median nucleotide identity across protein-coding loci). Using likelihood and Bayesian model discrimination methods, we rejected the strict maternal cotransmission hypothesis by showing a significant decoupling of symbiont and host mitochondrial (COI and mt16S genes) phylogenies. Indeed, decoupling occurred even when symB(VII) was excluded from phylogenetic reconstructions, suggesting a history of host switching in this group. Together, the data indicate a history of lateral symbiont transfer in vesicomyids, with symB(VII) being the most conspicuous example. Interpreted alongside previous studies of the vesicomyid symbiosis, these results suggest a mixed mode of symbiont transmission characterized by predominantly vertical transmission punctuated with instances of lateral symbiont acquisition. Lateral acquisition may facilitate the exchange of genetic material (recombination) among divergent symbiont lineages, rendering the evolutionary history of vesicomyid symbiont genomes much more complex than previously thought.