Advertisement

Environmental Science and Pollution Research

, Volume 22, Issue 20, pp 15347–15359 | Cite as

Substrates specialization in lipid compounds and hydrocarbons of Marinobacter genus

  • Patricia Bonin
  • Christophe Vieira
  • Régis Grimaud
  • Cécile Militon
  • Philippe Cuny
  • Oscar Lima
  • Sophie Guasco
  • Corina P. D. Brussaard
  • Valérie MichoteyEmail author
DECAPAGE Project: Hydrocarbon degradation in coastal sediments

Abstract

The impact of petroleum contamination and of burrowing macrofauna on abundances of Marinobacter and denitrifiers was tested in marine sediment mesocoms after 3 months incubation. Quantification of this genus by qPCR with a new primer set showed that the main factor favoring Marinobacter abundance was hydrocarbon amendment followed by macrofauna presence. In parallel, proportion of nosZ-harboring bacteria increased in the presence of marcrofauna. Quantitative finding were explained by physiological data from a set of 34 strains and by genomic analysis of 16 genomes spanning 15 different Marinobacter-validated species (Marinobacter hydrocarbonoclasticus, Marinobacter daeopensis, Marinobacter santoriniensis, Marinobacter pelagius, Marinobacter flavimaris, Marinobacter adhaerens, Marinobacter xestospongiae, Marinobacter algicola, Marinobacter vinifirmus, Marinobacter maritimus, Marinobacter psychrophilus, Marinobacter lipoliticus, Marinobacter manganoxydans, Marinobacter excellens, Marinobacter nanhaiticus) and 4 potential novel ones. Among the 105 organic electron donors tested in physiological analysis, Marinobacter pattern appeared narrow for almost all kinds of organic compounds except lipid ones. Strains of this set could oxidize a very large spectrum of lipids belonging to glycerolipids, branched, fatty acyls, and aromatic hydrocarbon classes. Physiological data were comforted by genomic analysis, and genes of alkane 1-monooxygenase, haloalkane dehalogenase, and flavin-binding monooxygenase were detected in most genomes. Denitrification was assessed for several strains belonging to M. hydrocarbonoclasticus, M. vinifirmus, Marinobacter maritinus, and M. pelagius species indicating the possibility to use nitrate as alternative electron acceptor. Higher occurrence of Marinobacter in the presence of petroleum appeared to be the result of a broader physiological trait allowing this genus to use lipids including hydrocarbon as principal electron donors.

Keywords

Marinobater Hydrocarbon Marine sediment Quantification Electron donor pattern Denitrification 

Notes

Acknowledgments

This work was supported by ANR (DECAPAGE ANR-11-CESA-0006). We thank the captain and shipboard crew of R/V Pelagia and scientific crew. Furthermore, we acknowledge the Royal Netherlands Institute for Sea Research (NIOZ) for the support by the NIOZ-Marine Research Facilities (MRF) on shore and on board.

Supplementary material

11356_2014_4009_MOESM1_ESM.pptx (89 kb)
ESM 1 (PPTX 88 kb)
11356_2014_4009_MOESM2_ESM.docx (38 kb)
ESM 2 (DOCX 37 kb)

References

  1. Abed RMM, Zein B, Al-Thukair A, de Beer D (2007) Phylogenetic diversity and activity of aerobic heterotrophic bacteria from a hypersaline oil-polluted microbial mat. Syst Appl Microbiol 30:319–330CrossRefGoogle Scholar
  2. Banta GT, Andersen O (2003) Bioturbation and the fate of sediment pollutants—experimental case studies of selected infauna species. Vie Milieu 53:233–248Google Scholar
  3. Baumann P, Baumann L (1981) The marine gram negative eubacteria genus Photobacterium, Beneckea, Alteromonas, Pseudomonas and Alcaligenes. In: S-V K (ed) The prokaryotes: a handbook on habitats, isolation and identification of bacteria. Mortimer, P. S, New York, pp 1302–1330Google Scholar
  4. Bonin P, Gilewicz M, Bertrand JC (1987) Denitrification by a marine bacterium pseudomonas-nautica strain-617. Ann Inst Pastur Mic 138:371–383CrossRefGoogle Scholar
  5. Bonin P, Gilewicz M, Bertrand JC (1992) Effects of oxygen on pseudomonas-nautica growth on N-alkane with or without nitrate. Arch Microbiol 157:538–545Google Scholar
  6. Bordenave S, Goni-Urriza MS, Caumette P, Duran R (2007) Effects of heavy fuel oil on the bacterial community structure of a pristine microbial mat. Appl Environ Microb 73:6089–6097CrossRefGoogle Scholar
  7. Bowman JP, McMeekin TA (2005) Marinobacter. In: Brenner DJ, Krieg NR, Staley JT (eds) Bergey’s manual of systematic bacteriology. Springer Science, New York, pp 459–463Google Scholar
  8. Bowman JP, McCammon SA, Brown MV, Nichols DS, McMeekin TA (1997) Diversity and association of psychrophilic bacteria in Antarctic sea ice. Appl Environ Microbiol 63:3068–3078Google Scholar
  9. Brito EM, Guyoneaud R, Goni-Urriza M, Ranchou-Peyruse A, Verbaere A, Crapez MAC, Wasserman JCA, Duran R (2006) Characterization of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay, Brazil. Res Microbiol 157:752–762CrossRefGoogle Scholar
  10. Canfield DE, Jorgensen BB, Fossing H, Glud R, Gundersen J, Ramsing NB, Thamdrup B, Hansen JW, Nielsen LP, Hall POJ (1993) Pathways of organic-carbon oxidation in 3 continental-margin sediments. Mar Geol 113:27–40CrossRefGoogle Scholar
  11. Canfield DE, Kristensen E, Thamdrup B (2005) Aquatic geomicrobiology. Adv Mar Biol 48:1–599CrossRefGoogle Scholar
  12. Cui ZS, Lai QL, Dong CM, Shao ZZ (2008) Biodiversity of polycyclic aromatic hydrocarbon-degrading bacteria from deep sea sediments of the Middle Atlantic Ridge. Environ Microbiol 10:2138–2149CrossRefGoogle Scholar
  13. Cui Z, Gao W, Xu G, Zheng L (2013) Genome sequence of the polycyclic aromatic hydrocarbon-degrading bacterium strain Marinobacter nanhaiticus D15-8WT. Genome Announc 1:e00301-13Google Scholar
  14. Deppe U, Richnow HH, Michaelis W, Antranikian G (2005) Degradation of crude oil by an arctic microbial consortium. Extremophiles 9:461–470CrossRefGoogle Scholar
  15. dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. Plos One: 6Google Scholar
  16. Doumenq P, Aries E, Asia L, Acquaviva M, Artaud J, Gilewicz M, Mille G, Bertrand JC (2001) Influence of n-alkanes and petroleum on fatty acid composition of a hydrocarbonoclastic bacterium: Marinobacter hydrocarbonoclasticus strain 617. Chemosphere 44:519–528CrossRefGoogle Scholar
  17. Duran R (2010) Marinobacter. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 1725–1735CrossRefGoogle Scholar
  18. Edwards KJ, Rogers DR, Wirsen CO, McCollom TM (2003) Isolation and characterization of novel psychrophilic, neutrophilic, Fe-oxidizing, chemolithoautotrophic alpha- and, gamma-Proteobacteria from the deep sea. Appl Environ Microbiol 69:2906–2913CrossRefGoogle Scholar
  19. Fernandes SO, Michotey VD, Guasco S, Bonin PC, Bharathi PAL (2012) Denitrification prevails over anammox in tropical mangrove sediments (Goa, India). Mar Environ Res 74:9–19CrossRefGoogle Scholar
  20. Gärdes A, Kaeppel E, Shehzad A, Seebah S, Teeling H, Yarza P, Glöckner F, Grossart H, Ullrich M (2010) Complete genome sequence of Marinobacter adhaerens type strain (HP15), a diatom-interacting marine microorganism. SIGS 3:97–107Google Scholar
  21. Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, Bertrand JC (1992) Marinobacter-hydrocarbonoclasticus Gen-Nov, Sp-Nov, a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576CrossRefGoogle Scholar
  22. Genovese M, Crisafi F, Denaro R, Cappello S, Russo D, Calogero R, Santisi S, Catalfamo M, Modica A, Smedile F, Genovese L, Golyshin PN, Giuliano L, Yakimov MM (2014) Effective bioremediation strategy for rapid in situ cleanup of anoxic marine sediments in mesocosm oil spill simulation. Front Microbiol: 5Google Scholar
  23. Gilewicz M, Nimatuzahroh NT, Budzinski H, Doumenq P, Michotey V, Bertrand JC (1997) Isolation and characterization of a marine bacterium capable of utilizing 2-methylphenanthrene. Appl Microbiol Biotechnol 48:528–533CrossRefGoogle Scholar
  24. Goregues C, Michotey V, Bonin P (2004) Isolation of hydrocarbonoclastic denitrifying bacteria from berre microbial mats. Ophelia 58:263–270CrossRefGoogle Scholar
  25. Goregues CM, Michotey VD, Bonin PC (2005) Molecular, biochemical, and physiological approaches for understanding the ecology of denitrification. Microb Ecol 49:198–208CrossRefGoogle Scholar
  26. Gorshkova NM, Ivanova EP, Sergeev AF, Zhukova NV, Alexeeva Y, Wright JP, Nicolau DV, Mikhailov VV, Christen R (2003) Marinobacter excellens sp nov., isolated from sediments of the Sea of Japan. Int J Syst Evol Microbiol 53:2073–2078CrossRefGoogle Scholar
  27. Gray ND, Sherry A, Grant RJ, Rowan AK, Hubert CRJ, Callbeck CM, Aitken CM, Jones DM, Adams JJ, Larter SR, Head IM (2011) The quantitative significance of Syntrophaceae and syntrophic partnerships in methanogenic degradation of crude oil alkanes. Environ Microbiol 13:2957–2975CrossRefGoogle Scholar
  28. Green DH, Bowman JP, Smith EA, Gutierrez T, Bolch CJS (2006) Marinobacter algicola sp nov., isolated from laboratory cultures of paralytic shellfish toxin-producing dinoflagellates. Int J Syst Evol Microbiol 56:523–527CrossRefGoogle Scholar
  29. Grimaud R (2010) Marinobacter. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin Heidelberg, pp 1289–1296CrossRefGoogle Scholar
  30. Grimaud R, Ghiglione JF, Cagnon C, Lauga B, Vaysse PJ, Rodriguez-Blanco A, Mangenot A, Cruveiller S, Barbe V, Duran R, Wu LF, Talla E, Bonin P, Michotey V (2012) Genome sequence of the marine bacterium Marinobacter hydrocarbonoclasticus SP17 which forms biofilms on hydrophobic organic compounds. J Bacteriol 94:3539–3540CrossRefGoogle Scholar
  31. Gu J, Cai H, Yu SL, Qu R, Yin B, Guo YF, Zhao JY, Wu XL (2007) Marinobacter gudaonensis sp nov., isolated from an oil-polluted saline soil in a Chinese oilfield. Int J Syst Evol Microbiol 57:250–254CrossRefGoogle Scholar
  32. Handley KM, Lloyd JR (2013) Biogeochemical implications of the ubiquitous colonization of marine habitats and redox gradients by Marinobacter species. Front Microbiol 4Google Scholar
  33. Handley KM, Upton M, Beatson S, Lloyd JR (2013) Genome sequence of thermal arsenic -respiring bacterium Marinobacter santoriniensis NKSG1. Genome Announc 1:e00231–13CrossRefGoogle Scholar
  34. Huu NB, Denner EBM, Ha DTC, Wanner G, Stan-Lotter H (1999) Marinobacter aquaeolei sp. nov., a halophilic bacterium isolated from a Vietnamese oil-producing well. Int J Syst Bacteriol 49:367–375CrossRefGoogle Scholar
  35. Karner M, Fuhrman JA (1997) Determination of active marine bacterioplankton: a comparison of universal 16S rRNA probes, autoradiography, and nucleoid staining. Appl Environ Microbiol 63:1208–1213Google Scholar
  36. Kim BY, Weon HY, Yoo SH, Kim JS, Kwon SW, Stackebrandt E, Go SJ (2006) Marinobacter koreensis sp nov., isolated from sea sand in Korea. Int J Syst Evol Microbiol 56:2653–2656CrossRefGoogle Scholar
  37. Ladygina N, Dedyukhina E, Vainshtein M (2006) A review on microbial synthesis of hydrocarbons. Process Biochem 41:1001–1014CrossRefGoogle Scholar
  38. Lamendella R, Strutt S, Borglin S, Chakraborty R, Tas N, Mason OU, Hultman J, Prestat E, Hazen TC, Jansson JK (2014) Assessments of the deepwater horizon oil spill impact on Gulf coast microbial communities. Front Microbiol 5Google Scholar
  39. Laverock B, Gilbert JA, Tait K, Osborn AM, Widdicombe S (2011) Bioturbation: impact on the marine nitrogen cycle. Biochem Soc T 39:315–320CrossRefGoogle Scholar
  40. Lee OO, Lai PY, Wu HX, Zhou XJ, Miao L, Wang H, Qian PY (2012) Marinobacter xestospongiae sp nov., isolated from the marine sponge Xestospongia testudinaria collected from the Red Sea. Int J Syst Evol Microbiol 62:1980–1985CrossRefGoogle Scholar
  41. Marquez MC, Ventosa A (2005) Marinobacter hydrocarbonoclasticus Gauthier et al. 1992 and Marinobacter aquaeolei Nguyen et al. 1999 are heterotypic synonyms. Int J Syst Evol Microbiol 55:1349–1351CrossRefGoogle Scholar
  42. Martin S, Marquez MC, Sanchez-Porro C, Mellado E, Arahal DR, Ventosa A (2003) Marinobacter lipolyticus sp nov., a novel moderate halophile with lipolytic activity. Int J Syst Evol Microbiol 53:1383–1387CrossRefGoogle Scholar
  43. Michotey V, Mejean V, Bonin P (2000) Comparison of methods for quantification of cytochrome cd(1)-denitrifying bacteria in environmental marine samples. Appl Environ Microbiol 66:1564–1571CrossRefGoogle Scholar
  44. Michotey V, Guasco S, Boeuf D, Morezzi N, Durieux B, Charpy L, Bonin P (2012) Spatio-temporal diversity of free-living and particle-attached prokaryotes in the tropical lagoon of Ahe atoll (Tuamotu Archipelago) and its surrounding oceanic waters. Mar Pollut Bull 65:525–537CrossRefGoogle Scholar
  45. Mikucki JA, Priscu JC (2007) Bacterial diversity associated with blood falls, a subglacial outflow from the Taylor Glacier, Antarctica. Appl Environ Microbiol 73:4029–4039CrossRefGoogle Scholar
  46. Nogales B, Timmis KN, Nedwell DB, Osborn AM (2002) Detection and diversity of expressed denitrification genes in estuarine sediments after reverse transcription-PCR amplification from mRNA. Appl Environ Microbiol 68:5017–5025CrossRefGoogle Scholar
  47. Papke RT, de la Haba R, Infante-Domínguez C, Pérez D, Sánchez-Porro C, Lapierre P, Ventosa A (2013) Draft genome sequence of the moderately halophilic bacterium Marinobacter lipolyticus strain SM19. Genome Announc 1:e00379–13CrossRefGoogle Scholar
  48. Romanenko LA, Schumann P, Rohde M, Zhukova NV, Mkhailov VV, Stackebrandt E (2005) Marinobacter bryozoorum sp nov and Marinobacter sediminum sp nov., novel bacteria from the marine environment. Int J Syst Evol Microbiol 55:143–148CrossRefGoogle Scholar
  49. Rontani JF, Gilewicz MJ, Michotey VD, Zheng TL, Bonin PC, Bertrand JC (1997) Aerobic and anaerobic metabolism of 6,10,14-trimethylpentadecan-2-one by a denitrifying bacterium isolated from marine sediments. Appl Environ Microbiol 63:636–643Google Scholar
  50. Rontani JF, Mouzdahir A, Michotey V, Bonin P (2002) Aerobic and anaerobic metabolism of squalene by a denitrifying bacterium isolated from marine sediment. Arch Microbiol 178:279–287CrossRefGoogle Scholar
  51. Rontani JF, Nassiry M, Michotey V, Guasco S, Bonin P (2010) Formation of pristane from alpha-tocopherol under simulated anoxic sedimentary conditions: a combination of biotic and abiotic degradative processes. Geochim Cosmochim Ac 74:252–263CrossRefGoogle Scholar
  52. Rosch C, Mergel A, Bothe H (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Appl Environ Microbiol 68:3818–3829CrossRefGoogle Scholar
  53. Seewald J (2003) Organic–inorganic interactions in petroleum-producing sedimentary basins. Nature 426:327–333CrossRefGoogle Scholar
  54. Shieh WY, Jean WD, Lin YT, Tseng M (2003) Marinobacter lutaoensis sp nov., a thermotolerant marine bacterium isolated from a coastal hot spring in Lutao, Taiwan. Can J Microbiol 49:244–252CrossRefGoogle Scholar
  55. Song L, Ren L, Li X, Yu D, Wang X, Liu G (2013) Complete genome sequence of Marinobacter sp.BSs20148. Genom a Genome Announc 1:e00236-13Google Scholar
  56. Sproer C, Lang E, Hobeck P, Burghardt J, Stackebrandt E, Tindall BJ (1998) Transfer of Pseudomonas nautica to Marinobacter hydrocarbonoclasticus. Int J Syst Bacteriol 48:1445–1448CrossRefGoogle Scholar
  57. Stauffert M, Cravo-Laureau C, Duran R (2014) Structure of hydrocarbonoclastic nitrate reducing bacterial communities in bioturbated coastal marine sediment. Fems Microbiol Ecol 89:580–593CrossRefGoogle Scholar
  58. Takai K, Moyer CL, Miyazaki M, Nogi Y, Hirayama H, Nealson KH, Horikoshi K (2005) Marinobacter alkaliphilus sp nov., a novel alkaliphilic bacterium isolated from subseafloor alkaline serpentine mud from ocean drilling program site 1200 at South Chamorro Seamount, mariana forearc. Extremophiles 9:17–27CrossRefGoogle Scholar
  59. Timmis KN (2010) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  60. Wang WP, Shao ZZ (2012) Diversity of flavin-binding monooxygenase genes (almA) in marine bacteria capable of degradation long-chain alkanes. Fems Microbiol Ecol 80:523–533CrossRefGoogle Scholar
  61. Wang H, Li H, Shao Z, Liao S, Johnstone L, Rensing C, Wang G (2012) Genome sequence of deep-sea Manganese-oxidizing bacterium Marinobacter manganoxydans MnI7-9. J Bacteriol 194:899–900CrossRefGoogle Scholar
  62. Welsh DT (2000) Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. Fems Microbiol Rev 24:263–290CrossRefGoogle Scholar
  63. Whiticar MJ, Suess E (1990) Hydrothremal hydrocarbon gases in the sediments of king George Basin, Branfield strait Antartica. Appl Geochem 5:135–147CrossRefGoogle Scholar
  64. Yakimov MM, Giuliano L, Crisafi E, Chernikova TN, Timmis KN, Golyshin PN (2002) Microbial community of a saline mud volcano at San Biagio-Belpasso, Mt. Etna (Italy). Environ Microbiol 4:249–256CrossRefGoogle Scholar
  65. Yoon JH, Yeo SH, Kim IG, Oh TK (2004) Marinobacter flavimaris sp nov and Marinobacter daepoensis sp nov., slightly halophilic organisms isolated from sea water of the Yellow Sea in Korea. Int J Syst Evol Microbiol 54:1799–1803CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Patricia Bonin
    • 1
  • Christophe Vieira
    • 1
    • 2
  • Régis Grimaud
    • 3
  • Cécile Militon
    • 1
  • Philippe Cuny
    • 1
  • Oscar Lima
    • 1
    • 4
  • Sophie Guasco
    • 1
  • Corina P. D. Brussaard
    • 5
  • Valérie Michotey
    • 1
    Email author
  1. 1.Aix Marseille Université, UM110, MIO CNRS IRDMarseilleFrance
  2. 2.Sorbonne Universités, UPMC Univ Paris 06, IFDParis cedex 05France
  3. 3.Institut Pluridisciplinaire de Recherche en Environnement et Matériaux, Equipe Environnement et Microbiologie, UMR 5254, CNRS, IBEASUniversité de Pau et des Pays de l’AdourPauFrance
  4. 4.Ecosystèmes, Biodiversité, Evolution (ECOBIO)CNRS : UMR6553 – Université de Rennes 1 – INEE – Observatoire des Sciences de l’Univers de RennesRennesFrance
  5. 5.Department of Biological OceanographyRoyal Netherlands Institute for Sea ResearchDen BurgNetherlands

Personalised recommendations