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Genomic and physiological analysis reveals versatile metabolic capacity of deep-sea Photobacterium phosphoreum ANT-2200

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Abstract

Bacteria of the genus Photobacterium thrive worldwide in oceans and show substantial eco-physiological diversity including free-living, symbiotic and piezophilic life styles. Genomic characteristics underlying this variability across species are poorly understood. Here we carried out genomic and physiological analysis of Photobacterium phosphoreum strain ANT-2200, the first deep-sea luminous bacterium of which the genome has been sequenced. Using optical mapping we updated the genomic data and reassembled it into two chromosomes and a large plasmid. Genomic analysis revealed a versatile energy metabolic potential and physiological analysis confirmed its growth capacity by deriving energy from fermentation of glucose or maltose, by respiration with formate as electron donor and trimethlyamine N-oxide (TMAO), nitrate or fumarate as electron acceptors, or by chemo-organo-heterotrophic growth in rich media. Despite that it was isolated at a site with saturated dissolved oxygen, the ANT-2200 strain possesses four gene clusters coding for typical anaerobic enzymes, the TMAO reductases. Elevated hydrostatic pressure enhances the TMAO reductase activity, mainly due to the increase of isoenzyme TorA1. The high copy number of the TMAO reductase isoenzymes and pressure-enhanced activity might imply a strategy developed by bacteria to adapt to deep-sea habitats where the instant TMAO availability may increase with depth.

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Abbreviations

TMAO:

Trimethylamine N-oxide

CDS:

Coding DNA sequence

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Acknowledgments

This work was supported by Grants SIDSSE-201307, SIDSSE-QN-201405, SIDSSE-QN-201406 and SIDSSE-QN-201408 from Sanya Institute of Deep-Sea Sciences and Engineering, the Strategic Priority Research Program grant XDB06010203 and International Partnership for Innovative Team Program (20140491526) from the Chinese Academy of Sciences, the NSFC 41506147 from National Natural Science Foundation of China, a grant for LIA-BioMNSL from Centre National de la Recherche Scientifique, the grant DY125-15-R-03 from China Ocean Mineral Resources R & D Association (COMRA) Special Foundation, the Grant NSFC 41306161 from the National Science Foundation of China and a grant from Mt. Tai Scholar Construction Engineering Special Foundation of Shandong Province. We acknowledge France Genomique for the support for this sequencing project.

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Authors and Affiliations

  1. Deep-Sea Microbial Cell Biology, Department of Deep Sea Sciences, Sanya Institute of Deep-Sea Science and Engineering, Chinese Academy of Sciences, Sanya, China

    Sheng-Da Zhang, Wei-Jia Zhang, Hai-Tao Chen, Xue-Gong Li & Qun-Jian Yin

  2. LCB UMR 7257, Aix-Marseille Université, CNRS, IMM, 31, Chemin Joseph Aiguier, 13402, Marseille Cedex 20, France

    Claire-Lise Santini, Charlotte Guyomar, François Alberto & Long-Fei Wu

  3. France-China Bio-Mineralization and Nano-Structure Laboratory (LIA-BioMNSL), LCB-CNRS, Marseille, France/SIDSSE-CAS, Sanya, China

    Sheng-Da Zhang, Claire-Lise Santini, Wei-Jia Zhang, Charlotte Guyomar, Hai-Tao Chen, Xue-Gong Li, Qun-Jian Yin, François Alberto & Long-Fei Wu

  4. DSV/IG/Genoscope/LF, CEA, Evry, France

    Valérie Barbe & Sophie Mangenot

  5. Aix-Marseille Université, Université du Sud Toulon-Var, CNRS/INSU, IRD, Mediterranean Institute of Oceanography (MIO), UM110, 13288, Marseille, France

    Marc Garel, Séverine Martini, Nathalie Pradel & Christian Tamburini

  6. Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China

    Yuan Zhao

  7. DSV, iBEB/SBTN, CEA, Bagnols-sur-Cèze, France

    Jean Armengaud, Jean-Charles Gaillard & Claude Vidaud

  8. Laboratoire d’Analyse Bioinformatique en Génomique et Métabolisme, CEA/DSV/IG/Genoscope and CNRS-UMR 8030 and Univ. Evry Val d’Esssone, Evry, France

    Claudine Médigue

Authors
  1. Sheng-Da Zhang
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  2. Claire-Lise Santini
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  3. Wei-Jia Zhang
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  11. Yuan Zhao
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  16. Claude Vidaud
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  17. François Alberto
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  18. Claudine Médigue
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  19. Christian Tamburini
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  20. Long-Fei Wu
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Corresponding author

Correspondence to Long-Fei Wu.

Additional information

Communicated by H. Atomi.

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Zhang, SD., Santini, CL., Zhang, WJ. et al. Genomic and physiological analysis reveals versatile metabolic capacity of deep-sea Photobacterium phosphoreum ANT-2200. Extremophiles 20, 301–310 (2016). https://doi.org/10.1007/s00792-016-0822-1

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  • DOI: https://doi.org/10.1007/s00792-016-0822-1

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