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
The
Zetaproteobacteria
are a class of bacteria typically associated with marine Fe(II)-oxidizing environments. First discovered in the hydrothermal vents at Loihi Seamount, Hawaii, they have become model organisms for marine microbial Fe(II) oxidation. In addition to deep sea and shallow hydrothermal vents,
Zetaproteobacteria
are found in coastal sediments, other marine subsurface environments, steel corrosion biofilms and saline terrestrial springs. Isolates from a range of environments all grow by autotrophic Fe(II) oxidation. Their success lies partly in their microaerophily, which enables them to compete with abiotic Fe(II) oxidation at Fe(II)-rich oxic/anoxic transition zones. To determine the known diversity of the
Zetaproteobacteria
, we have used 16S rRNA gene sequences to define 59 operational taxonomic units (OTUs), at 97% similarity. While some
Zetaproteobacteria
taxa appear to be cosmopolitan, others are enriched by specific habitats. OTU networks show that certain
Zetaproteobacteria
co-exist, sharing compatible niches. These niches may correspond with adaptations to O
2
, H
2
and nitrate availability, based on genomic analyses of metabolic potential. Also, a putative Fe(II) oxidation gene has been found in diverse
Zetaproteobacteria
taxa, suggesting that the
Zetaproteobacteria
evolved as Fe(II) oxidation specialists. In all, studies suggest that
Zetaproteobacteria
are widespread, and therefore may have a broad influence on marine and saline terrestrial Fe cycling.
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