Molecular phylogenetic and isotopic evidence of two lineages of chemoautotrophic endosymbionts distinct at the subdivision level harbored in one host-animal type: The genus Alviniconcha (Gastropoda: Provannidae)

Authors

  • Yohey Suzuki,

    Corresponding author
    1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237–0061, Japan
      *Corresponding author. Tel.: +81 46 867 9710; fax: +81 46 867 9715., E-mail address: yohey@jamstec.go.jp
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  • Takenori Sasaki,

    1. Department of Historical Geology and Paleontology, The University Museum, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113–0033, Japan
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  • Masae Suzuki,

    1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237–0061, Japan
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  • Shinji Tsuchida,

    1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237–0061, Japan
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  • Kenneth H. Nealson,

    1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237–0061, Japan
    2. Department of Earth Sciences, University of Southern California, 3651 Trousdale Pkwy., Los Angeles, CA 90089–0740, USA
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  • Koki Horikoshi

    1. Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237–0061, Japan
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  • Edited by Dr. A. Oren

*Corresponding author. Tel.: +81 46 867 9710; fax: +81 46 867 9715., E-mail address: yohey@jamstec.go.jp

Abstract

The hydrothermal-vent gastropod Alviniconcha hessleri from the Alice Springs deep-sea hydrothermal field in the Mariana Back-Arc Basin in the Western Pacific houses an intracellular bacterial endosymbiont in its gill. Although enzymatic analysis has revealed that the endosymbiont is a sulfur-oxidizing chemoautotroph using the Calvin–Benson cycle for the fixation of carbon dioxide, the phylogenetic affiliation of, and the trophic relationship of A. hessleri with, the chemoautotrophic endosymbiont remains undetermined. A single 16S rRNA gene sequence was obtained from the DNA extract of the gill, and phylogenetic analysis placed the source organism within the lineage of the gamma subdivision of the Proteobacteria that consists of many chemoautotrophic endosymbionts of marine invertebrates. Fluorescence in situ hybridization analysis showed the bacterium densely colonizing the gill filaments. The fatty acid profile of the symbiont-free mantle contains the high level of the 16:1 fatty acid originating from the endosymbiont, which indicates that the endosymbiont cells are digested by, and incorporated into, the host. Compound-specific carbon isotopic analysis revealed that fatty acids from the gastropod tissues are all 13C-depleted relative to the gastropod biomass. This fractionation pattern is consistent with chemoautotrophy based on the Calvin–Benson cycle and subsequent fatty-acid biosynthesis from 13C-depleted acetyl coenzyme A. The results from the present study are clearly different from those from our previous study for A. aff. hessleri from the Indian Ocean that harbors a chemoautotrophic endosymbiont belonging to the epsilon subdivision of the Proteobacteria, which mediates the reductive tricarboxylic acid cycle for carbon fixation. Thus, it is concluded here that two lineages of chemoautotrophic bacteria, phylogenetically distinct at the subdivision level, occur as the primary endosymbiont in one host-animal type, which is unknown for the other metazoans.

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