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Expression of genes for sulfur oxidation in the intracellular chemoautotrophic symbiont of the deep-sea bivalve Calyptogena okutanii

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Abstract

To understand sulfur oxidation in thioautotrophic deep-sea clam symbionts, we analyzed the recently reported genomes of two chemoautotrophic symbionts of Calyptogena okutanii (Candidatus Vesicomyosocius okutanii strain HA: Vok) and C. magnifica (Candidatus Ruthia magnifica strain Cm: Rma), and examined the sulfur oxidation gene expressions in the Vok by RT-PCR. Both symbionts have genes for sulfide-quinone oxidoreductase (sqr), dissimilatory sulfite reductase (dsr), reversible dissimilatory sulfite reductase (rdsr), sulfur-oxidizing multienzyme system (sox) (soxXYZA and soxB but lacking soxCD), adenosine phosphosulfate reductase (apr), and ATP sulfurylase (sat). While these genomes share 29 orthologous genes for sulfur oxidation implying that both symbionts possess the same sulfur oxidation pathway, Rma has a rhodanese-related sulfurtransferase putative gene (Rmag0316) that has no corresponding ortholog in Vok, and Vok has one unique dsrR (COSY0782). We propose that Calyptogena symbionts oxidize sulfide and thiosulfate, and that sulfur oxidation proceeds as follows. Sulfide is oxidized to sulfite by rdsr. Sulfite is oxidized to sulfate by apr and sat. Thiosulfate is oxidized to zero-valence sulfur by sox, which is then reduced to sulfide by dsr. In addition, thiosulfate may also be oxidized into sulfate by another component of sox. The result of the RT-PCR showed that genes (dsrA, dsrB, dsrC, aprA, aprB, sat, soxB, and sqr) encoding key enzymes catalyzing sulfur oxidation were all equally expressed in the Vok under three different environmental conditions (aerobic, semioxic, and aerobic under high pressure at 9 MPa), indicating that all sulfur oxidation pathways function simultaneously to support intracellular symbiotic life.

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Acknowledgments

We are grateful to the captains and crew of the R/V Natsushima and R/V Yokosuka and to the operation teams of the DSRV Shinkai6500 and ROV Hyperdolphin for sample collection. We thank Drs. K. Takai, T. Nunoura, and Y. Fujiwara at JAMSTEC and H. Kojima at Hokkaido University for their discussion. We also thank M. Kawato at JAMSTEC for the help with DNA sequencing and Dr. P. Kottapalli for helpful comments.

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Authors and Affiliations

  1. Marine Biodiversity Research Program, Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka, 237-0061, Japan

    Maiko Harada, Takao Yoshida, Hirokazu Kuwahara, Shigeru Shimamura, Yoshihiro Takaki, Chiaki Kato, Tetsuya Miwa & Tadashi Maruyama

  2. Graduate School of Biosystem Studies, Tsukuba University, Tsukuba, Ibaraki, 305-8572, Japan

    Maiko Harada

  3. Department of Marine Biosciences, School of Marine Biosciences, Kitasato University, Ofunato, Iwate, 022-0101, Japan

    Hiroshi Miyake

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  1. Maiko Harada
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  2. Takao Yoshida
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  3. Hirokazu Kuwahara
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  4. Shigeru Shimamura
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  5. Yoshihiro Takaki
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  9. Tadashi Maruyama
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Correspondence to Takao Yoshida.

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Communicated by A. Driessen.

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Harada, M., Yoshida, T., Kuwahara, H. et al. Expression of genes for sulfur oxidation in the intracellular chemoautotrophic symbiont of the deep-sea bivalve Calyptogena okutanii . Extremophiles 13, 895–903 (2009). https://doi.org/10.1007/s00792-009-0277-8

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  • DOI: https://doi.org/10.1007/s00792-009-0277-8

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