Solar-panel and parasol strategies shape the proteorhodopsin distribution pattern in marine Flavobacteriia

Yohei Kumagai, Susumu Yoshizawa, Yu Nakajima, Mai Watanabe, Tsukasa Fukunaga, Yoshitoshi Ogura, Tetsuya Hayashi, Kenshiro Oshima, Masahira Hattori, Masahiko Ikeuchi, Kazuhiro Kogure, Edward F. DeLong, Wataru Iwasaki

    Research output: Contribution to journalArticle

    2 Citations (Scopus)

    Abstract

    Proteorhodopsin (PR) is a light-driven proton pump that is found in diverse bacteria and archaea species, and is widespread in marine microbial ecosystems. To date, many studies have suggested the advantage of PR for microorganisms in sunlit environments. The ecophysiological significance of PR is still not fully understood however, including the drivers of PR gene gain, retention, and loss in different marine microbial species. To explore this question we sequenced 21 marine Flavobacteriia genomes of polyphyletic origin, which encompassed both PR-possessing as well as PR-lacking strains. Here, we show that the possession or alternatively the lack of PR genes reflects one of two fundamental adaptive strategies in marine bacteria. Specifically, while PR-possessing bacteria utilize light energy (“solar-panel strategy”), PR-lacking bacteria exclusively possess UV-screening pigment synthesis genes to avoid UV damage and would adapt to microaerobic environment (“parasol strategy”), which also helps explain why PR-possessing bacteria have smaller genomes than those of PR-lacking bacteria. Collectively, our results highlight the different strategies of dealing with light, DNA repair, and oxygen availability that relate to the presence or absence of PR phototrophy.

    Original languageEnglish
    Pages (from-to)1-15
    Number of pages15
    JournalISME Journal
    DOIs
    Publication statusAccepted/In press - 2018 Feb 6

    Fingerprint

    solar collectors
    rhodopsin
    bacterium
    Bacteria
    gene
    bacteria
    genome
    photoautotrophy
    repair
    distribution
    proteorhodopsin
    pigment
    Phototrophic Processes
    pump
    microorganism
    Solar Energy
    Genome
    Genes
    Light
    DNA

    ASJC Scopus subject areas

    • Microbiology
    • Ecology, Evolution, Behavior and Systematics

    Cite this

    Kumagai, Y., Yoshizawa, S., Nakajima, Y., Watanabe, M., Fukunaga, T., Ogura, Y., ... Iwasaki, W. (Accepted/In press). Solar-panel and parasol strategies shape the proteorhodopsin distribution pattern in marine Flavobacteriia. ISME Journal, 1-15. https://doi.org/10.1038/s41396-018-0058-4

    Solar-panel and parasol strategies shape the proteorhodopsin distribution pattern in marine Flavobacteriia. / Kumagai, Yohei; Yoshizawa, Susumu; Nakajima, Yu; Watanabe, Mai; Fukunaga, Tsukasa; Ogura, Yoshitoshi; Hayashi, Tetsuya; Oshima, Kenshiro; Hattori, Masahira; Ikeuchi, Masahiko; Kogure, Kazuhiro; DeLong, Edward F.; Iwasaki, Wataru.

    In: ISME Journal, 06.02.2018, p. 1-15.

    Research output: Contribution to journalArticle

    Kumagai, Y, Yoshizawa, S, Nakajima, Y, Watanabe, M, Fukunaga, T, Ogura, Y, Hayashi, T, Oshima, K, Hattori, M, Ikeuchi, M, Kogure, K, DeLong, EF & Iwasaki, W 2018, 'Solar-panel and parasol strategies shape the proteorhodopsin distribution pattern in marine Flavobacteriia' ISME Journal, pp. 1-15. https://doi.org/10.1038/s41396-018-0058-4
    Kumagai, Yohei ; Yoshizawa, Susumu ; Nakajima, Yu ; Watanabe, Mai ; Fukunaga, Tsukasa ; Ogura, Yoshitoshi ; Hayashi, Tetsuya ; Oshima, Kenshiro ; Hattori, Masahira ; Ikeuchi, Masahiko ; Kogure, Kazuhiro ; DeLong, Edward F. ; Iwasaki, Wataru. / Solar-panel and parasol strategies shape the proteorhodopsin distribution pattern in marine Flavobacteriia. In: ISME Journal. 2018 ; pp. 1-15.
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    abstract = "Proteorhodopsin (PR) is a light-driven proton pump that is found in diverse bacteria and archaea species, and is widespread in marine microbial ecosystems. To date, many studies have suggested the advantage of PR for microorganisms in sunlit environments. The ecophysiological significance of PR is still not fully understood however, including the drivers of PR gene gain, retention, and loss in different marine microbial species. To explore this question we sequenced 21 marine Flavobacteriia genomes of polyphyletic origin, which encompassed both PR-possessing as well as PR-lacking strains. Here, we show that the possession or alternatively the lack of PR genes reflects one of two fundamental adaptive strategies in marine bacteria. Specifically, while PR-possessing bacteria utilize light energy (“solar-panel strategy”), PR-lacking bacteria exclusively possess UV-screening pigment synthesis genes to avoid UV damage and would adapt to microaerobic environment (“parasol strategy”), which also helps explain why PR-possessing bacteria have smaller genomes than those of PR-lacking bacteria. Collectively, our results highlight the different strategies of dealing with light, DNA repair, and oxygen availability that relate to the presence or absence of PR phototrophy.",
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    AU - Fukunaga, Tsukasa

    AU - Ogura, Yoshitoshi

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    AU - Hattori, Masahira

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