Abstract
BackgroundDeep-sea mussels harboring chemoautotrophic symbionts from hydrothermal vents and seeps are assumed to have evolved from shallow-water asymbiotic relatives by way of biogenic reducing environments such as sunken wood and whale falls. Such symbiotic associations have been well characterized in mussels collected from vents, seeps and sunken wood but in only a few from whale falls.Methodology/Principal FindingHere we report symbioses in the gill tissues of two mussels, Adipicola crypta and Adipicola pacifica, collected from whale-falls on the continental shelf in the northwestern Pacific. The molecular, morphological and stable isotopic characteristics of bacterial symbionts were analyzed. A single phylotype of thioautotrophic bacteria was found in A. crypta gill tissue and two distinct phylotypes of bacteria (referred to as Symbiont A and Symbiont C) in A. pacifica. Symbiont A and the A. crypta symbiont were affiliated with thioautotrophic symbionts of bathymodiolin mussels from deep-sea reducing environments, while Symbiont C was closely related to free-living heterotrophic bacteria. The symbionts in A. crypta were intracellular within epithelial cells of the apical region of the gills and were extracellular in A. pacifica. No spatial partitioning was observed between the two phylotypes in A. pacifica in fluorescence in situ hybridization experiments. Stable isotopic analyses of carbon and sulfur indicated the chemoautotrophic nature of A. crypta and mixotrophic nature of A. pacifica. Molecular phylogenetic analyses of the host mussels showed that A. crypta constituted a monophyletic clade with other intracellular symbiotic (endosymbiotic) mussels and that A. pacifica was the sister group of all endosymbiotic mussels.Conclusions/SignificanceThese results strongly suggest that the symbiosis in A. pacifica is at an earlier stage in evolution than other endosymbiotic mussels. Whale falls and other modern biogenic reducing environments may act as refugia for primal chemoautotrophic symbioses between eukaryotes and prokaryotes since the extinction of ancient large marine vertebrates.
Highlights
Deep-sea bathymodiolin mussels (Bivalvia: Mytilidae) thrive in reducing environments such as hydrothermal vents, hydrocarbon seeps, whale falls and sunken wood and have chemoautotrophic and/or methanotrophic symbiotic relationships with proteobacteria [1,2,3,4,5,6,7,8,9,10,11,12,13]
Symbiont-harboring deep-sea mussels are hypothesized to have derived from asymbiotic shallow-water relatives by way of sunken wood falls, which were proposed to act as evolutionary stepping-stones for the introduction of chemoautotrophy-dependent invertebrates into vent and seep environments based on the results of molecular phylogenetic analyses of mytilid mussels [18]
In A. pacifica, the bacteria were located on the apical surfaces of epithelial cells of the gills (Fig. 1A)
Summary
Deep-sea bathymodiolin mussels (Bivalvia: Mytilidae) thrive in reducing environments such as hydrothermal vents, hydrocarbon seeps, whale falls and sunken wood and have chemoautotrophic and/or methanotrophic symbiotic relationships with proteobacteria [1,2,3,4,5,6,7,8,9,10,11,12,13]. Symbiont-harboring deep-sea mussels (primarily subfamily Bathymodiolinae) are hypothesized to have derived from asymbiotic shallow-water relatives by way of sunken wood falls, which were proposed to act as evolutionary stepping-stones for the introduction of chemoautotrophy-dependent invertebrates into vent and seep environments based on the results of molecular phylogenetic analyses of mytilid mussels [18]. Deep-sea mussels harboring chemoautotrophic symbionts from hydrothermal vents and seeps are assumed to have evolved from shallow-water asymbiotic relatives by way of biogenic reducing environments such as sunken wood and whale falls. Such symbiotic associations have been well characterized in mussels collected from vents, seeps and sunken wood but in only a few from whale falls
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