Distribution, phylogenetic diversity and physiological characteristics of epsilon-Proteobacteria in a deep-sea hydrothermal field

Authors

  • Satoshi Nakagawa,

    Corresponding author
    1. Laboratory of Marine Microbiology, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Oiwake-cho, Kitashirakawa, Kyoto 606-8502, Japan.
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    • Present address: Subground Animalcule Retrieval (SUGAR) Project, Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.

  • Ken Takai,

    1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
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  • Fumio Inagaki,

    1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
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  • Hisako Hirayama,

    1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
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  • Takuro Nunoura,

    1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
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  • Koki Horikoshi,

    1. Subground Animalcule Retrieval (SUGAR) Project, Frontier Research System for Extremophiles, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan.
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  • Yoshihiko Sako

    1. Laboratory of Marine Microbiology, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Oiwake-cho, Kitashirakawa, Kyoto 606-8502, Japan.
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*E-mail nakagawas@jamstec.go.jp; Tel. (+81) 46 867 9694; Fax (+81) 46 867 9715.

Summary

Epsilon-Proteobacteria is increasingly recognized as an ecologically significant group of bacteria, particularly in deep-sea hydrothermal environments. In this study, we studied the spatial distribution, diversity and physiological characteristics of the epsilon-Proteobacteria in various microbial habitats in the vicinity of a deep-sea hydrothermal vent occurring in the Iheya North field in the Mid-Okinawa Trough, by using culture-dependent and -independent approaches. The habitats studied were inside and outside hydrothermal plume, and annelid polychaete tubes. In addition, we deployed colonization devices near the vent emission. The polychaete tubes harboured physiologically and phylogenetically diverse microbial community. The in situ samplers were predominantly colonized by epsilon-Proteobacteria. Energy metabolism of epsilon-Proteobacteria isolates was highly versatile. Tree topology generated from the metabolic traits was significantly different (P = 0.000) from that of 16S rRNA tree, indicating current 16S rRNA gene-based analyses do not provide sufficient information to infer the physiological characteristics of epsilon-Proteobacteria. Nevertheless, culturability of epsilon-Proteobacteria in various microbial habitats differed among the phylogenetic subgroups. Members of Sulfurimonas were characterized by the robust culturability, and the other phylogenetic subgroups appeared to lose culturability in seawater, probably because of the sensitivity to oxygen. These results provide new insight into the ecophysiological characteristics of the deep-sea hydrothermal vent epsilon-Proteobacteria, which has never been assessed by comparative analysis of the 16S rRNA genes.

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