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Extremophiles

, Volume 20, Issue 3, pp 301–310 | Cite as

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

  • Sheng-Da Zhang
  • Claire-Lise Santini
  • Wei-Jia Zhang
  • Valérie Barbe
  • Sophie Mangenot
  • Charlotte Guyomar
  • Marc Garel
  • Hai-Tao Chen
  • Xue-Gong Li
  • Qun-Jian Yin
  • Yuan Zhao
  • Jean Armengaud
  • Jean-Charles Gaillard
  • Séverine Martini
  • Nathalie Pradel
  • Claude Vidaud
  • François Alberto
  • Claudine Médigue
  • Christian Tamburini
  • Long-Fei WuEmail author
Original Paper

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.

Keywords

Deep-sea adaptation Bioluminescence TMAO reductase Hydrostatic pressure Anaerobic respiration 

Abbreviations

TMAO

Trimethylamine N-oxide

CDS

Coding DNA sequence

Notes

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.

Supplementary material

792_2016_822_MOESM1_ESM.docx (4.5 mb)
Supplementary material 1 (DOCX 4601 kb)

References

  1. Abe F, Kato C, Horikoshi K (1999) Pressure-regulated metabolism in microorganisms. Trends Microbiol 7:447–453CrossRefPubMedGoogle Scholar
  2. AlAli B, Garel M, Cuny P, Miquel JC, Toubal T, Robert A, Tamburini C (2010) Luminous bacteria in the deep-sea waters near the ANTARES underwater neutrino telescope (Mediterranean Sea). Chem Ecol 26:57–72CrossRefGoogle Scholar
  3. Ansaldi M, Simon G, Lepelletier M, Mejean V (2000) The TorR high-affinity binding site plays a key role in both torR autoregulation and torCAD operon expression in Escherichia coli. J Bacteriol 182:961–966CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ansaldi M, Jourlin-Castelli C, Lepelletier M, Theraulaz L, Mejean V (2001) Rapid dephosphorylation of the TorR response regulator by the TorS unorthodox sensor in Escherichia coli. J Bacteriol 183:2691–2695CrossRefPubMedPubMedCentralGoogle Scholar
  5. Armengaud J, Trapp J, Pible O, Geffard O, Chaumot A, Hartmann EM (2014) Non-model organisms, a species endangered by proteogenomics. J Proteomics 105:5–18CrossRefPubMedGoogle Scholar
  6. Ast JC, Dunlap PV (2005) Phylogenetic resolution and habitat specificity of members of the Photobacterium phosphoreum species group. Environ Microbiol 7:1641–1654CrossRefPubMedGoogle Scholar
  7. Bordi C, Ansaldi M, Gon S, Jourlin-Castelli C, Iobbi-Nivol C, Mejean V (2004) Genes regulated by TorR, the trimethylamine oxide response regulator of Shewanella oneidensis. J Bacteriol 186:4502–4509CrossRefPubMedPubMedCentralGoogle Scholar
  8. Campanaro S et al (2005) Laterally transferred elements and high pressure adaptation in Photobacterium profundum strains. BMC Genomics 6:122CrossRefPubMedPubMedCentralGoogle Scholar
  9. Christie-Oleza JA, Fernandez B, Nogales B, Bosch R, Armengaud J (2012) Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J 6:124–135CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dryselius R, Kurokawa K, Iida T (2007) Vibrionaceae, a versatile bacterial family with evolutionarily conserved variability. Res Microbiol 158:479–486CrossRefPubMedGoogle Scholar
  11. El-Hajj ZW, Allcock D, Tryfona T, Lauro FM, Sawyer L, Bartlett DH, Ferguson GP (2010) Insights into piezophily from genetic studies on the deep-sea bacterium, Photobacterium profundum SS9. Ann N Y Acad Sci 1189:143–148CrossRefPubMedGoogle Scholar
  12. Eloe EA, Lauro FM, Vogel RF, Bartlett DH (2008) The deep-sea bacterium Photobacterium profundum SS9 utilizes separate flagellar systems for swimming and swarming under high-pressure conditions. Appl Envionment Microbiol 74:6298–6305CrossRefGoogle Scholar
  13. Frankel RB, Bazylinski DA, Johnson MS, Taylor BL (1997) Magneto-aerotaxis in marine coccoid bacteria. Biophys J 73:994–1000CrossRefPubMedPubMedCentralGoogle Scholar
  14. Genest O, Ilbert M, Mejean V, Iobbi-Nivol C (2005) TorD, an essential chaperone for TorA molybdoenzyme maturation at high temperature. J Biol Chem 280:15644–15648CrossRefPubMedGoogle Scholar
  15. Le Bihan T, Rayner J, Roy MM, Spagnolo L (2013) Photobacterium profundum under pressure: a MS-based label-free quantitative proteomics study. PLoS One 8:e60897CrossRefPubMedPubMedCentralGoogle Scholar
  16. Martini S et al (2013) Effects of hydrostatic pressure on growth and luminescence of a moderately-piezophilic luminous bacteria Photobacterium phosphoreum ANT-2200. PLoS One 8:e66580CrossRefPubMedPubMedCentralGoogle Scholar
  17. Okada K, Iida T, Kita-Tsukamoto K, Honda T (2005a) Vibrios commonly possess two chromosomes. J Bacteriol 187:752–757CrossRefPubMedPubMedCentralGoogle Scholar
  18. Okada K, Iida T, Kita-Tsukamoto K, Honda T (2005b) Vibrios commonly possess two chromosomes. J Bacteriol 187:752–757CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ruan J et al (2012) Architecture of a flagellar apparatus in the fast-swimming magnetotactic bacterium MO-1. Proc Natl Acad Sci USA 109:20643–20648CrossRefPubMedPubMedCentralGoogle Scholar
  20. Santini CL, Ize B, Chanal A, Muller M, Giordano G, Wu LF (1998) A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J 17:101–112CrossRefPubMedPubMedCentralGoogle Scholar
  21. Simon G, Jourlin C, Ansaldi M, Pascal MC, Chippaux M, Mejean V (1995) Binding of the TorR regulator to cis-acting direct repeats activates tor operon expression. Mol Microbiol 17:971–980CrossRefPubMedGoogle Scholar
  22. Tamburini C et al (2013) Deep-sea bioluminescence blooms after dense water formation at the ocean surface. PLoS One 8:e67523CrossRefPubMedPubMedCentralGoogle Scholar
  23. Urbanczyk H et al (2011) Genome sequence of Photobacterium mandapamensis strain svers.1.1, the bioluminescent symbiont of the cardinal fish Siphamia versicolor. J Bacteriol 193:3144–3145CrossRefPubMedPubMedCentralGoogle Scholar
  24. Vallenet D et al (2013) MicroScope–an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res 41:D636–D647CrossRefPubMedPubMedCentralGoogle Scholar
  25. Vezzi A et al (2005) Life at depth: Photobacterium profundum genome sequence and expression analysis. Science 307:1459–1461CrossRefPubMedGoogle Scholar
  26. Wang F et al (2008) Environmental adaptation: genomic analysis of the piezotolerant and psychrotolerant deep-sea iron reducing bacterium Shewanella piezotolerans WP3. PLoS One 3:e1937CrossRefPubMedPubMedCentralGoogle Scholar
  27. Welch TJ, Bartlett DH (1998) Identification of a regulatory protein required for pressure-responsive gene expression in the deep-sea bacterium Photobacterium species strain SS9. Mol Microbiol 27:977–985CrossRefPubMedGoogle Scholar
  28. Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Living with water stress: evolution of osmolyte systems. Science 217:1214–1222CrossRefPubMedGoogle Scholar
  29. Yancey PH, Blake WR, Conley J (2002) Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants. Comp Biochem Physiol A: Mol Integr Physiol 133:667–676CrossRefGoogle Scholar
  30. Yancey PH, Gerringer ME, Drazen JC, Rowden AA, Jamieson A (2014) Marine fish may be biochemically constrained from inhabiting the deepest ocean depths. Proc Natl Acad Sci USA 111:4461–4465CrossRefPubMedPubMedCentralGoogle Scholar
  31. Zhang WJ et al (2012) Complex spatial organization and flagellin composition of flagellar propeller from marine magnetotactic ovoid strain MO-1. J Mol Biol 416:558–570CrossRefPubMedGoogle Scholar
  32. Zhang SD et al (2014a) Genome sequence of luminous piezophile Photobacterium phosphoreum ANT-2200. Genome Announc 2:e00096–14PubMedPubMedCentralGoogle Scholar
  33. Zhang SD et al (2014b) Swimming behaviour and magnetotaxis function of the marine bacterium strain MO-1. Environ Microbiol Rep 6:14–20CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Sheng-Da Zhang
    • 1
    • 3
  • Claire-Lise Santini
    • 2
    • 3
  • Wei-Jia Zhang
    • 1
    • 3
  • Valérie Barbe
    • 4
  • Sophie Mangenot
    • 4
  • Charlotte Guyomar
    • 2
    • 3
  • Marc Garel
    • 5
  • Hai-Tao Chen
    • 1
    • 3
  • Xue-Gong Li
    • 1
    • 3
  • Qun-Jian Yin
    • 1
    • 3
  • Yuan Zhao
    • 6
  • Jean Armengaud
    • 7
  • Jean-Charles Gaillard
    • 7
  • Séverine Martini
    • 5
  • Nathalie Pradel
    • 5
  • Claude Vidaud
    • 7
  • François Alberto
    • 2
    • 3
  • Claudine Médigue
    • 8
  • Christian Tamburini
    • 5
  • Long-Fei Wu
    • 2
    • 3
    Email author
  1. 1.Deep-Sea Microbial Cell Biology, Department of Deep Sea Sciences, Sanya Institute of Deep-Sea Science and EngineeringChinese Academy of SciencesSanyaChina
  2. 2.LCB UMR 7257, Aix-Marseille Université, CNRS, IMMMarseille Cedex 20France
  3. 3.France-China Bio-Mineralization and Nano-Structure Laboratory (LIA-BioMNSL), LCB-CNRS, Marseille, France/SIDSSE-CASSanyaChina
  4. 4.DSV/IG/Genoscope/LF, CEAEvryFrance
  5. 5.Aix-Marseille Université, Université du Sud Toulon-Var, CNRS/INSU, IRD, Mediterranean Institute of Oceanography (MIO), UM110MarseilleFrance
  6. 6.Key Laboratory of Marine Ecology and Environmental Sciences, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  7. 7.DSV, iBEB/SBTN, CEABagnols-sur-CèzeFrance
  8. 8.Laboratoire d’Analyse Bioinformatique en Génomique et Métabolisme, CEA/DSV/IG/Genoscope and CNRS-UMR 8030 and Univ. Evry Val d’EsssoneEvryFrance

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