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The Marine Isolate Novosphingobium sp. PP1Y Shows Specific Adaptation to Use the Aromatic Fraction of Fuels as the Sole Carbon and Energy Source

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Abstract

Novosphingobium sp. PP1Y, isolated from a surface seawater sample collected from a closed bay in the harbour of Pozzuoli (Naples, Italy), uses fuels as its sole carbon and energy source. Like some other Sphingomonads, this strain can grow as either planktonic free cells or sessile-aggregated flocks. In addition, this strain was found to grow as biofilm on several types of solid and liquid hydrophobic surfaces including polystyrene, polypropylene and diesel oil. Strain PP1Y is not able to grow on pure alkanes or alkane mixtures but is able to grow on a surprisingly wide range of aromatic compounds including mono, bi, tri and tetracyclic aromatic hydrocarbons and heterocyclic compounds. During growth on diesel oil, the organic layer is emulsified resulting in the formation of small biofilm-coated drops, whereas during growth on aromatic hydrocarbons dissolved in paraffin the oil layer is emulsified but the drops are coated only if the mixtures contain selected aromatic compounds, like pyrene, propylbenzene, tetrahydronaphthalene and heterocyclic compounds. These peculiar characteristics suggest strain PP1Y has adapted to efficiently grow at the water/fuel interface using the aromatic fraction of fuels as the sole carbon and energy source.

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References

  1. Baird WM, Hooven LA, Mahadevan B (2005) Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ Mol Mutagen 45:106–114

    Article  PubMed  CAS  Google Scholar 

  2. Balkwill DL, Drake GR, Reeves RH, Fredrickson JK, White DC, Ringelberg DB, Chandler DP, Romine MF, Kennedy DW, Spadoni CM (1997) Taxonomic study of aromatic-degrading bacteria from deep-terrestrial-subsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov. Int J Syst Bacteriol 47:191–201

    Article  PubMed  CAS  Google Scholar 

  3. Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from antarctic soil. Microb Ecol 43:44–54

    Article  PubMed  CAS  Google Scholar 

  4. Beynon RJ, Oliver S (1996) Avoidance of proteolysis in extracts. In: Doonan S (ed) Protein purification protocols, vol 59. Humana, Totowa, pp 81–94

    Chapter  Google Scholar 

  5. Black JA, Birge WJ, Westerman AG, Francis PC (1983) Comparative aquatic toxicology of aromatic hydrocarbons. Fundam Appl Toxicol 3:353–358

    Article  PubMed  CAS  Google Scholar 

  6. Brennan ML, Wu W, Fu X, Shen Z, Song W, Frost H, Vadseth C, Narine L, Lenkiewicz E, Borchers MT, Lusis AJ, Lee JJ, Lee NA, Abu-Soud HM, Ischiropoulos H, Hazen SL (2002) A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem 277:17415–17427, Epub 2002 Feb 27

    Article  PubMed  CAS  Google Scholar 

  7. Coppotelli BM, Ibarrolaza A, Dias RL, Del Panno MT, Berthe-Corti L, Morelli IS (2010) Study of the degradation activity and the strategies to promote the bioavailability of phenanthrene by Sphingomonas paucimobilis strain 20006FA. Microb Ecol 59:266–276

    Article  PubMed  CAS  Google Scholar 

  8. Davison AD, Gillings MR, Jardine DR, Karuso P, Nouwens AS, French JJ, Veal DA, Altavilla N (1999) Sphingomonas paucimobilis BPSI-3 mutant AN2 produces a red catabolite during biphenyl degradation. J Ind Microbiol Biotechnol 23:314–319

    Article  PubMed  CAS  Google Scholar 

  9. Desai AM, Autenrieth RL, Dimitriou-Christidis P, McDonald TJ (2008) Biodegradation kinetics of select polycyclic aromatic hydrocarbon (PAH) mixtures by Sphingomonas paucimobilis EPA505. Biodegradation 19:223–233, Epub 2007 May 30

    Article  PubMed  CAS  Google Scholar 

  10. Golyshin PN, Chernikova TN, Abraham WR, Lunsdorf H, Timmis KN, Yakimov MM (2002) Oleiphilaceae fam. nov., to include Oleiphilus messinensis gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 52:901–911

    Article  PubMed  CAS  Google Scholar 

  11. Handa N (1966) Examination on the applicability of the Phenol SulfuricAcid method to the determination of dissolved carbohydrate in sea water. J Oceanogr Soc Jpn 22:79–86

    Google Scholar 

  12. Henry JA (1998) Composition and toxicity of petroleum products and their additives. Hum Exp Toxicol 17:111–123

    Article  PubMed  CAS  Google Scholar 

  13. Jenkins CL, Andrewes AG, McQuade TJ, Starr MP (1979) The pigment of Pseudomonas paucimobilis is a carotenoid (Nostoxanthin), rather than a brominated aryl-polyene (xanthomonadin). Curr Microbiol 3:1–4

    Article  CAS  Google Scholar 

  14. Kaminski M, Gilgenast E, Przyjazny A, Romanik G (2006) Procedure for and results of simultaneous determination of aromatic hydrocarbons and fatty acid methyl esters in diesel fuels by high performance liquid chromatography. J Chromatogr A 1122:153–160

    Article  PubMed  CAS  Google Scholar 

  15. Kaminski M, Kartanowicz R, Przyjazny A (2004) Application of high-performance liquid chromatography with ultraviolet diode array detection and refractive index detection to the determination of class composition and to the analysis of gasoline. J Chromatogr A 1029:77–85

    Article  PubMed  CAS  Google Scholar 

  16. Kawahara K, Kuraishi H, Zahringer U (1999) Chemical structure and function of glycosphingolipids of Sphingomonas spp and their distribution among members of the alpha-4 subclass of proteobacteria. J Ind Microbiol Biotechnol 23:408–413

    Article  PubMed  CAS  Google Scholar 

  17. Kertesz MA, Kawasaki A (2010) Hydrocarbon-degrading sphingomonads: Sphingomonas, Sphingobium, Novosphingobium, and Sphingopyxis. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol. Springer, Berlin, pp 1693–1705

    Chapter  Google Scholar 

  18. Kim IS, Ryu JY, Hur HG, Gu MB, Kim SD, Shim JH (2004) Sphingomonas sp. strain SB5 degrades carbofuran to a new metabolite by hydrolysis at the furanyl ring. J Agric Food Chem 52:2309–2314

    Article  PubMed  CAS  Google Scholar 

  19. Kim SJ, Kweon O, Cerniglia CE (2010) Degradation of polycyclic aromatic hydrocarbons by Mycobacterium strains. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol. Springer, Berlin, pp 1865–1879

    Chapter  Google Scholar 

  20. King RW (1988) Petroleum: its composition, analysis and processing. Occup Med 3:409–430

    PubMed  CAS  Google Scholar 

  21. Liang F, Lu M, Keener TC, Liu Z, Khang SJ (2005) The organic composition of diesel particulate matter, diesel fuel and engine oil of a non-road diesel generator. J Environ Monit 7:983–988, Epub 2005 Aug 8

    Article  PubMed  CAS  Google Scholar 

  22. Liu ZP, Wang BJ, Liu YH, Liu SJ (2005) Novosphingobium taihuense sp. nov., a novel aromatic-compound-degrading bacterium isolated from Taihu Lake, China. Int J Syst Evol Microbiol 55:1229–1232

    Article  PubMed  CAS  Google Scholar 

  23. Mackey AP, Hodgkinson M (1996) Assessment of the impact of naphthalene contamination on mangrove fauna using behavioral bioassays. Bull Environ Contam Toxicol 56:279–286

    Article  PubMed  CAS  Google Scholar 

  24. McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176

    Article  PubMed  CAS  Google Scholar 

  25. Mueller JG, Chapman PJ, Blattmann BO, Pritchard PH (1990) Isolation and characterization of a fluoranthene-utilizing strain of Pseudomonas paucimobilis. Appl Environ Microbiol 56:1079–1086

    PubMed  CAS  Google Scholar 

  26. Östman CE, Colmsjö AL (1988) Retention characteristics of alkylated polycyclic aromatic hydrocarbons in normal phase liquid chromatography. Chromatographia 25:25–30

    Article  Google Scholar 

  27. Palleroni NJ, Pieper DH, Moore ERB (2010) Microbiology of hydrocarbon-degrading Pseudomonas. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol. Springer, Berlin, pp 1787–1798

    Chapter  Google Scholar 

  28. Ramos JL, Duque E, Gallegos MT, Godoy P, Ramos-Gonzalez MI, Rojas A, Teran W, Segura A (2002) Mechanisms of solvent tolerance in gram-negative bacteria. Annu Rev Microbiol 56:743–768, Epub 2002 Jan 30

    Article  PubMed  CAS  Google Scholar 

  29. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  30. Sawyer RF (1993) Trends in auto emissions and gasoline composition. Environ Health Perspect 101:5–12

    PubMed  CAS  Google Scholar 

  31. Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Puhler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorholter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004

    Article  PubMed  CAS  Google Scholar 

  32. Seth-Smith H (2010) ‘Slick’ operation. Nat Rev Microbiol 8:538

    Article  PubMed  CAS  Google Scholar 

  33. Shimada T (2006) Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab Pharmacokinet 21:257–276

    Article  PubMed  CAS  Google Scholar 

  34. Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    PubMed  CAS  Google Scholar 

  35. Sohn JH, Kwon KK, Kang JH, Jung HB, Kim SJ (2004) Novosphingobium pentaromativorans sp. nov., a high-molecular-mass polycyclic aromatic hydrocarbon-degrading bacterium isolated from estuarine sediment. Int J Syst Evol Microbiol 54:1483–1487

    Article  PubMed  CAS  Google Scholar 

  36. Staley JT (2010) Cycloclasticus: A genus of marine polycyclic aromatic hydrocarbon degrading bacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol. Springer, Berlin, pp 1781–1786

    Chapter  Google Scholar 

  37. Stolz A (2009) Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81:793–811, Epub 2008 Nov 11

    Article  PubMed  CAS  Google Scholar 

  38. Story SP, Kline EL, Hughes TA, Riley MB, Hayasaka SS (2004) Degradation of aromatic hydrocarbons by Sphingomonas paucimobilis strain EPA505. Arch Environ Contam Toxicol 47:168–176

    Article  PubMed  CAS  Google Scholar 

  39. Stringfellow WT, Aitken MD (1995) Competitive metabolism of naphthalene, methylnaphthalenes, and fluorene by phenanthrene-degrading pseudomonads. Appl Environ Microbiol 61:357–362

    PubMed  CAS  Google Scholar 

  40. Teira E, Lekunberri I, Gasol JM, Nieto-Cid M, Alvarez-Salgado XA, Figueiras FG (2007) Dynamics of the hydrocarbon-degrading Cycloclasticus bacteria during mesocosm-simulated oil spills. Environ Microbiol 9:2551–2562

    Article  PubMed  CAS  Google Scholar 

  41. Toren A, Orr E, Paitan Y, Ron EZ, Rosenberg E (2002) The active component of the bioemulsifier alasan from Acinetobacter radioresistens KA53 is an OmpA-like protein. J Bacteriol 184:165–170

    Article  PubMed  CAS  Google Scholar 

  42. Wang Z, Fingas M, Blenkinsopp S, Sergy G, Landriault M, Sigouin L, Foght J, Semple K, Westlake DW (1998) Comparison of oil composition changes due to biodegradation and physical weathering in different oils. J Chromatogr A 809:89–107

    Article  PubMed  CAS  Google Scholar 

  43. Yabuuchi E, Yamamoto H, Terakubo S, Okamura N, Naka T, Fujiwara N, Kobayashi K, Kosako Y, Hiraishi A (2001) Proposal of Sphingomonas wittichii sp. nov. for strain RW1T, known as a dibenzo-p-dioxin metabolizer. Int J Syst Evol Microbiol 51:281–292

    PubMed  CAS  Google Scholar 

  44. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266, Epub 2007 May 9

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are indebted to Prof. Maurilio De Felice, Università di Napoli Federico II, for critically reading the manuscript.

This work was supported by a grant from the Ministry of University and Research (PRIN/2007).

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Correspondence to Eugenio Notomista.

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Notomista, E., Pennacchio, F., Cafaro, V. et al. The Marine Isolate Novosphingobium sp. PP1Y Shows Specific Adaptation to Use the Aromatic Fraction of Fuels as the Sole Carbon and Energy Source. Microb Ecol 61, 582–594 (2011). https://doi.org/10.1007/s00248-010-9786-3

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