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ISME J. 2018 May;12(5):1329-1343. doi: 10.1038/s41396-018-0058-4. Epub 2018 Feb 6.

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

Author information

1
Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, 277-8564, Japan.
2
Department of Natural Environmental Studies, Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8563, Japan.
3
Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, 277-8564, Japan. yoshizawa@aori.u-tokyo.ac.jp.
4
Department of Natural Environmental Studies, Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8563, Japan. yoshizawa@aori.u-tokyo.ac.jp.
5
Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, 153-8902, Japan.
6
Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8561, Japan.
7
Department of Bacteriology, Faculty of Medical Sciences, Kyushu University, Fukuoka, 812-8582, Japan.
8
Center for Omics and Bioinformatics, Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8561, Japan.
9
Graduate School of Advanced Science and Engineering, Waseda University, Tokyo, 169-8555, Japan.
10
Center for Microbial Oceanography: Research and Education, University of Hawaii, Honolulu, HI, 96822, USA.
11
Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, 277-8564, Japan. iwasaki@bs.s.u-tokyo.ac.jp.
12
Department of Computational Biology and Medical Sciences, Graduate School of Frontier Sciences, The University of Tokyo, Chiba, 277-8561, Japan. iwasaki@bs.s.u-tokyo.ac.jp.
13
Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, 113-0032, Japan. iwasaki@bs.s.u-tokyo.ac.jp.

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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