Evidence for the role of endosymbionts in regional-scale habitat partitioning by hydrothermal vent symbioses

Abstract

Deep-sea hydrothermal vents are populated by dense communities of animals that form symbiotic associations with chemolithoautotrophic bacteria. To date, our understanding of which factors govern the distribution of host/symbiont associations (or holobionts) in nature is limited, although host physiology often is invoked. In general, the role that symbionts play in habitat utilization by vent holobionts has not been thoroughly addressed. Here we present evidence for symbiont-influenced, regional-scale niche partitioning among symbiotic gastropods (genus Alviniconcha) in the Lau Basin. We extensively surveyed Alviniconcha holobionts from four vent fields using quantitative molecular approaches, coupled to characterization of high-temperature and diffuse vent-fluid composition using gastight samplers and in situ electrochemical analyses, respectively. Phylogenetic analyses exposed cryptic host and symbiont diversity, revealing three distinct host types and three different symbiont phylotypes (one ε-proteobacteria and two γ-proteobacteria) that formed specific associations with one another. Strikingly, we observed that holobionts with ε-proteobacterial symbionts were dominant at the northern fields, whereas holobionts with γ-proteobacterial symbionts were dominant in the southern fields. This pattern of distribution corresponds to differences in the vent geochemistry that result from deep subsurface geological and geothermal processes. We posit that the symbionts, likely through differences in chemolithoautotrophic metabolism, influence niche utilization among these holobionts. The data presented here represent evidence linking symbiont type to habitat partitioning among the chemosynthetic symbioses at hydrothermal vents and illustrate the coupling between subsurface geothermal processes and niche availability. chemoautotrophy | symbiosis | endosymbiosis

Molecular taxonomy and naming of five cryptic species ofAlviniconchasnails (Gastropoda: Abyssochrysoidea) from hydrothermal vents

“…Suzuki et al, 2005a;Suzuki et al, 2005b). The differences might result from associations with different endosymbiont types (e-versus g-proteobacteria) (e.g., Beinart et al, 2012), but resolution of this problem is significantly beyond the scope of the present study. We observed considerable variation in several shell characters, especially the height of the spire (Fig.…”

“…type I. (Beinart et al, 2012;Kojima, Fujikura, Okutani, & Hashimoto, 2004;Kojima et al, 2001;Kojima et al, 1998;Sievert, H€ ugler, Taylor, & Wirsen, 2008;Suzuki et al, 2006a;Urakawa et al, 2005). Alviniconcha cf.…”

“…No reliable conclusions about morphological differences could be drawn from our material because only limited tissue remained for most of our specimens. COMMENT: Alviniconcha boucheti harbours epsilonproteobacterial endosymbionts within vacuoles in the ctenidia (Beinart et al, 2012;Suzuki et al, 2006a). DISTRIBUTION: Known from hydrothermal vent localities at 1300 to 2700 m depths in the Manus, Fiji and Lau basins, in the Western Pacific.…”

“…COMMENT: Alviniconcha kojimai harbours both epsilonand gamma-proteobacterial endosymbionts within vacuoles in the ctenidia (Beinart et al, 2012;Suzuki et al, 2006a;Urakawa et al, 2005). DISTRIBUTION: Known from hydrothermal vent localities at 1480-to 2700 m depths in the Manus, Fiji and Lau basins, in the Western Pacific.…”

Vent Fauna on the Central Indian Ridge

“…The large, hairy Alviniconcha snails, which also host bacterial symbionts, are dominant in the vent fields of the Mariana Trough, and in the southernmost vent fields of the western Pacific region, but are less abundant in the Indian Ocean. Several lineages of these gastropods have been detected using molecular approaches (Kojima et al 2001;Beinart et al 2012). However, the taxonomic description of this species is still in progress, and only provisional names are used.…”