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Analysis of the composition of bacterial communities in oil reservoirs from a southern offshore Brazilian basin

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Abstract

The aim of this study was to characterize and compare the bacterial community structure of two distinct oil samples from a petroleum field in Brazil by using both molecular, based on the construction of 16S rRNA gene libraries, and cultivation methods. Statistical comparisons of libraries based on Amplified Ribosomal DNA Restriction Analysis (ARDRA) data revealed no significant differences between the communities recovered in the non-biodegraded (NBD) and highly biodegraded oils (HBD). BlastN analysis of the 16S rRNA gene sequences representative of distinct ribotypes from both oils showed the presence of nine different bacterial genera in these samples, encompassing members of the genera Arcobacter, Halanaerobium, Marinobacter, Propionibacterium, Streptomyces, Leuconostoc, Acinetobacter, Bacillus and Streptococcus. Enrichments obtained using oil as inoculum and sole carbon source yielded bacterial isolates showing high 16S rRNA gene sequence similarity with Achromobacter xylosoxidans, Bacillus subtilis, Brevibacillus sp., Dietzia sp. and Methylobacterium sp. Comparison between the data obtained using cultivation-independent and enrichment cultures suggests that different selection of community members may occur when using distinct approaches. All the organisms found, except for Leuconostoc sp. and Streptococus sp., have been previously reported in the literature as hydrocarbon degraders and/or associated to oil field environments.

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References

  • Al-Sharidah A, Richardt A, Golecki JR, Dierstein R, Tadros MH (2000) Isolation and characterization of two hydrocarbon-degrading Bacillus subtilis strains from oil contaminated soil of Kuwait. Microbiol Res 155:157–164

    PubMed  CAS  Google Scholar 

  • Asmus HE, Ponte FC (1973) The Brazilian marginal basins. In: Nairn AE, Sthli FG (eds) The ocean basins and margins, vol. 1, South Atlantic, Plenun Press, New York, pp 87–133

    Google Scholar 

  • Bach H, Berdichevsky Y, Gutnick D (2003) An exocellular protein from the oil-degrading microbe Acinetobacter venetianus RAG-1 enhances the emulsifying activity of the polymeric bioemulsifier emulsan. Appl Environ Microbiol 69:2608–2615

    Article  PubMed  CAS  Google Scholar 

  • Bachoon DS, Araujo R, Molina M, Hodson RE (2001) Microbial community dynamics and evaluation of bioremediation strategies in oil-impacted salt marsh sediment microcosms. J Ind Microbiol Biotechnol 27:72–79

    Article  PubMed  CAS  Google Scholar 

  • Barbeau K, Zhang G, Live DH, Butler A (2002) Petrobactin, a photoreactive siderophore produced by the oil-degrading marine bacterium Marinobacter hydrocarbonoclasticus. J Am Chem Soc 124:378–379

    Article  PubMed  CAS  Google Scholar 

  • Barkovskii AL, Shub GM (1986) Acinetobacter calcoaceticus strain with a wide spectrum of utilizing aromatic compounds and carrying a plasmid for resorcin degradation. Mikrobiologiia 55(2):237–240

    PubMed  CAS  Google Scholar 

  • Batrakov SG, Rodionova TA, Esipov SE, Polyakov NB, Sheichenko VI, Shekhovtsova NV, Lukin SM, Panikov NS, Nikolaev YA (2003) A novel lipopeptide, an inhibitor of bacterial adhesion, from the thermophilic and halotolerant subsurface Bacillus licheniformis strain 603. Biochim Biophys Acta 1634(3):107–150

    PubMed  CAS  Google Scholar 

  • Behlülgil K, Mehmetogelu MT (2002) Bacteria for improvement of oil recovery: a laboratory study. Energy Sources 24:413–421

    Article  Google Scholar 

  • Bieszkiewicz E, Horoch M, Boszczyk-Maleszak H, Mycielski R (1998) An attempt to use selected strains of bacteria adapted to high concentrations of petroleum oil to increase the effective removal of petroleum products in excess activated sludge in laboratory conditions. Acta Microbiol Pol 47:305–312

    PubMed  CAS  Google Scholar 

  • Bhupathiraju VK, Oren A, Sharma PK, Tanner RS, Woese CR, McInerney MJ (1994) Haloanaerobium salsugo sp. nov., a moderately halophilic, anaerobic bacterium from a subterranean brine. Int J Syst Bacteriol 44(3):565–572

    PubMed  CAS  Google Scholar 

  • Bonch-Osmolovskaya EA, Miroshnichenko ML, Lebedinsky AV, Chernyh NA, Nazina TN, Ivoilov VS, Belyaev SS, Boulygina ES, Lysov YP, Perov AN, Mirzabekov AD, Hippe H, Stackebrandt E, L’Haridon S, Jeanthon C (2003) Radioisotopic, culture-based, and oligonucleotide microchip analyses of thermophilic microbial communities in a continental high-temperature petroleum reservoir. Appl Environ Microbiol 69:6143–6151

    Article  PubMed  CAS  Google Scholar 

  • Chaillan F, Le Fleche A, Bury E, Phantavong YH, Grimont P, Saliot A, Oudot J (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155:587–595

    Article  PubMed  CAS  Google Scholar 

  • Chandler DP, Shu-Mei L, Spadoni CM, Drake GR, Balkwill DL, Fredrickson JK, Brockman FJ (1997) A molecular comparison of culturable aerobic heterotrophic bacteria and 16S rDNA clones derived from a deep subsurface sediment. FEMS Microbiol Ecol 23:131–144

    Article  CAS  Google Scholar 

  • Connan J (1984) In: Brooks J, Welte DH (eds) Advances in petroleum geochemistry, vol 1. Academic, London, pp 299–335

  • Damelin LH, Dykes A, von Holy A (1995) Biodiversity of lactic acid bacteria from food-related ecosystems. Microbios 83:13–22

    PubMed  CAS  Google Scholar 

  • DeLong EF (1992) Archaea in coastal marine environments. Proceedings of the Natural Academy of Sciences USA 89:5685–5689

    Article  CAS  Google Scholar 

  • 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 44:519–528

    Article  PubMed  CAS  Google Scholar 

  • Eilers H, Pernthaler J, Glockner FO, Amann R (2000) Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microbiol 66(7):3044–3051

    Article  PubMed  CAS  Google Scholar 

  • 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(4):568–576

    PubMed  CAS  Google Scholar 

  • Gevertz D, Telang AJ, Voordouw G, Jenneman GE (2000) Isolation and characterization of strains CVO and FWKO B, two novel nitrate-reducing, sulfide-oxidizing bacteria isolated from oil field brine. Appl Environ Microbiol 66(6):2491–2501

    Article  PubMed  CAS  Google Scholar 

  • Gotelli NJ, Entsminger GL (2003) EcoSim: null models software for ecology. Acquired Intelligence Inc. & Kesey-Bear, Burlington, VT 05465

  • Guardado LR, Gamboa LAP, Lucchesi CF (1989) Petroleum geology of the Campos Basin, Brazil, a model for a producing Atlantic type basin. In: Edwards JD, Santogrossi PA (eds) Divergent/passive margin basins, AAPG Memoir 48, 3–79

  • Head IM, Jones DM, Larter SR (2003) Biological activity in the deep subsurface and the origin of heavy oil. Nature 426:344–352

    Article  PubMed  CAS  Google Scholar 

  • Hugenholtz P, Goebel BM, Pace NR (1998) Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J Bacteriol 180:4765–4774

    PubMed  CAS  Google Scholar 

  • Huu NB, Denner EB, Ha DT, 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(2):367–375

    PubMed  CAS  Google Scholar 

  • Jahnert R, França A, Trindade LAF, Quintaes C, Santos P, Pessoa J, Bedregal RP (1998) The petroleum system of Campos Basin. BGP; AAPG International Conference & Exhibition, November 8–11, 1998, Rio de Janeiro, Brasil. Extended abstracts volume, 600–601

  • Jarvis GN, Strompl C, Moore ER, Thiele JH (1998) Isolation and characterisation of obligately anaerobic, lipolytic bacteria from the rumen of red deer. Syst Appl Microbiol 21:135–143

    PubMed  CAS  Google Scholar 

  • Juck D, Charles T, Whyte LG, Greer CW (2000) Polyphasic microbial community analysis of petroleum hydrocarbon-contaminated oils from two northern Canadian communities. FEMS Microbiol Ecol 33:241–249

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA Sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. John Wiley & Sons, Chichester, England, pp 115–175

  • Larter S, Wilhelms A, Head IM, Koopmans M, Aplin R, Di Primio R, Zwach C, Erdmann M, Telnaes N (2003) The controls on the composition of biodegraded oils in the deep subsurface – part 1: biodegradation rates in petroleum reservoirs. Org Geochem 34:601–613

    Article  CAS  Google Scholar 

  • Larter S, Huang H, Adams J, Bennett B, Jokanola O, Oldemburg T, Jones M, Head I, Riediger C, Fowler M (2006) The controls on the composition of biodegraded oils in the deep subsurface – part II: geological controls on subsurface biodegradation fluxes and constraints on reservoir fluid property prediction. AAPG Bull 90:921–938

    Article  CAS  Google Scholar 

  • Lu XX, Zhang X, Li GH, Zhang WH (2003) Production of biosurfactant and its role in the biodegradation of oil hydrocarbons. J Environ Sci Health A Tox Hazard Subst Environ Eng 38:483–492

    Article  PubMed  CAS  Google Scholar 

  • Magot M, Ollivier B, Patel BKC (2000) Microbiology of petroleum reservoirs. Ant Van Leeuwen 77:103–116

    Article  CAS  Google Scholar 

  • Mohiak WU, Mello MR, Karner GD, Dewey JF, Maxwell JR (1989) Structural and stratigraphic evolution of the Campos Basin, offshore Brazil. Extentional Tectonics and Stratigraphy of North Atlantic Margins: Analogs, AAPG Memoir 46:577–598

    Google Scholar 

  • Munson MA, Nedwell DB, Embley TM (1997) Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh. Appl Environ Microbiol 63:4729–4733

    PubMed  CAS  Google Scholar 

  • Nazina TN, Grigor’ian AA, Sue KF, Sokolova DSh, Novikova EV, Turova TP, Poltaraus AB, Beliaev SS, Ivanov MV (2002) Phylogenetic diversity of aerobic saprotrophic bacteria isolated from the Daqing oil field. Mikrobiologiia 71:103–110

    PubMed  CAS  Google Scholar 

  • Orphan VJ, Taylor LT, Hafenbradl D, Delong EF (2000) Culture-dependent and culture-independent characterization of microbial assemblage associated with high temperature petroleum reservoirs. Appl Environ Microbiol 66:700–711

    Article  PubMed  CAS  Google Scholar 

  • Pace NR (1996) New perspective on the natural microbial world: molecular microbial ecology. ASM News 62:463–470

    Google Scholar 

  • Peters KE, Moldowan JM (1993) The Biomarkers Guide. Prentice-Hall, New York, 363 pp

    Google Scholar 

  • Pettersson B, Lembke F, Hammer P, Stackebrandt E, Priest FG (1996) Bacillus sporothermodurans, a new species producing highly heat-resistant endospores. Int J Syst Bacteriol 46(3):759–764

    PubMed  CAS  Google Scholar 

  • Pineda-Flores G, Boll-Arguello G, Lira-Galeana C, Mesta-Howard AM (2004) A microbial consortium isolated from a crude oil sample that uses asphaltenes as a carbon and energy source. Biodegradation 15:145–151

    Article  PubMed  CAS  Google Scholar 

  • Pleshakova EV, Muratova AIu, Turkovskaia OV (2001) Degradation of mineral oil by Acinetobacter calcoaceticus strain. Prikl Biokhim Mikrobiol 37:398–404

    PubMed  CAS  Google Scholar 

  • Ponte FC, Asmus HE (1978) Geological framework of the Brazilian continental margin. Geol Rundsch 67:201–235

    Article  Google Scholar 

  • Radwan SS, Sorkhoh NA, Fardoun F, Al-Hasan RH (1995) Soil management enhancing hydrocarbon biodegradation in the polluted Kuwaiti desert. Appl Microbiol Biotechnol 44(1–2):265–270

    PubMed  CAS  Google Scholar 

  • Radwan SS, Barabas G, Sorkhoh NA, Damjanovich S, Szabo I, Szollosi J, Matko J, Penyige A, Hirano T, Szabo IM (1998) Hydrocarbon uptake by Streptomyces. FEMS Microbiol Lett 169(1):87–94

    Article  PubMed  CAS  Google Scholar 

  • Rainey FA, Ward-Reiney N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: Proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092

    Article  PubMed  CAS  Google Scholar 

  • Rangel HD, Martins FAL, Esteves FR, Feijó FJ (1994) Bacia de Campos. Boletim de Geociências da Petrobras 8(1):203–217

    Google Scholar 

  • Ravot G, Magot M, Ollivier B, Patel BK, Ageron E, Grimont PA, Thomas P, Garcia JL (1997) Haloanaerobium congolense sp. nov., an anaerobic, moderately halophilic, thiosulfate- and sulfur-reducing bacterium from an African oil field. FEMS Microbiol Lett 147(1):81–88

    Article  PubMed  CAS  Google Scholar 

  • Saadoun I (2002) Isolation and characterization of bacteria from crude petroleum oil contaminated soil and their potential to degrade diesel fuel. J Basic Microbiol 42:420–428

    Article  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Small-scale preparations of plasmid DNA. In: Molecular cloning: a laboratory manual, 2nd edn., vol 1. Cold Spring Harbor Laboratory Press, Plainview, NY, pp 25–30

  • Schink B (1997) Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev 61:262–280

    PubMed  CAS  Google Scholar 

  • Stapleton RD, Bright NG, Sayler GS (2000) Catabolic and genetic diversity of degradative bacteria from fuel-hydrocarbon contaminated aquifers. Microb Ecol 39(3):211–221

    PubMed  CAS  Google Scholar 

  • Stephen JR, McCaig AE, Smith Z, Prosser JI, Embley TM (1996) Molecular diversity of soil and marine 16S rRNA gene sequences related to beta-subgroup ammonia-oxidizing bacteria. Appl Environ Microbiol 62:4147–4154

    PubMed  CAS  Google Scholar 

  • Stiles ME, Holzapfel WH (1997) Lactic acid bacteria for foods and their current taxonomy. Review article Int J Food Microbiol 36:1–29

    Article  PubMed  CAS  Google Scholar 

  • Sugimori D, Nakamura M, Mihara Y (2002) Microbial degradation of lipid by Acinetobacter sp. strain SOD-1. Biosci Biotechnol Biochem 66(7):1579–1582

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2000) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Takami H, Inoue A, Fuji F, Horikoshi K (1997) Microbial flora in the deepest sea mud of the Mariana Trench. FEMS Microbiol Lett 152:279–285

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Sogabe M, Okumura K, Kurane R (2002) A highly selective direct method of detecting sulphate-reducing bacteria in crude oil. Lett Appl Microbiol 35:242–246

    Article  PubMed  CAS  Google Scholar 

  • Teske A, Sigalevich P, Cohen Y, Muyzer G (1996) Molecular identification of bacteria from a coculture by denaturing gradient gel electrophoresis of 16S ribosomal DNA fragments as a tool for isolation in pure cultures. Appl Environ Microbiol 62(11):4210–4215

    PubMed  CAS  Google Scholar 

  • Thamdrup B, Rossello-Mora R, Amann R (2000) Microbial manganese and sulfate reduction in Black Sea shelf sediments. Appl Environ Microbiol 66(7):2888–2897

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • Tyrrell GJ, Lovgren M, Kress B, Grimsrud K (2005) Invasive Group A streptococcal disease in Alberta, Canada, 2000–2002. J Clin Microbiol 43:1678–1683

    Article  PubMed  Google Scholar 

  • Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol. Mol. Biol. Rev. 67:503–549

    Article  PubMed  CAS  Google Scholar 

  • Vepritskiy AA, Vitol IA, Nierzwicki-Bauer SA (2002) Novel group I intron in the tRNA(Leu)(UAA) gene of a gamma-proteobacterium isolated from a deep subsurface environment. J Bacteriol 184:1481–1487

    Article  PubMed  CAS  Google Scholar 

  • von Wintzingerode F, Goebel UB, Stackebrandt E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21:219–233

    Article  Google Scholar 

  • Vorob’eva LI, Kraeva NI, Ebringer L, Ol’sinskaia NL (1979) n-Alkane oxidation by propionic acid bacteria. Mikrobiologiia 48:33–38

    PubMed  CAS  Google Scholar 

  • Voordouw G, Armstrong SM, Reimer MF, Fouts B, Telang AJ, Shen Y, Gevertz D (1996) Characterization of 16S rRNA genes from oil field microbial communities indicates the presence of a variety of sulfate-reducing, fermentative, and sulfide-oxidizing bacteria. Appl. Environ. Microbiol. 62:1623–1629

    PubMed  CAS  Google Scholar 

  • Watanabe K, Watanabe K, Kodama Y, Syutsubo K, Harayama S (2000) Molecular characterization of bacterial populations in petroleum-contaminated groundwater discharged from underground crude oil storage cavities. Appl Environ Microbiol 66:4803–4809

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Kodama Y, Hamamura N, Kaku N (2002) Diversity, abundance, and activity of archaeal populations in oil-contaminated groundwater accumulated at the bottom of an underground crude oil storage cavity. Appl Environ Microbiol 68:3899–3907

    Article  PubMed  CAS  Google Scholar 

  • Yoshida N, Yagi K, Sato D, Watanabe N, Kuroishi T, Nishimoto K, Yanagida A, Katsuragi T, Kanagawa T, Kurane R, Tani Y (2005) Bacterial communities in petroleum oil in stockpiles. J Biosci Bioeng 99:143–149

    Article  PubMed  CAS  Google Scholar 

  • Young A, Blakesley R (1991) Sequencing plasmids form single colonies with the dsDNA cycle sequencing system. Focus 13:13

    Google Scholar 

  • Zhuang WQ, Tay JH, Maszenan AM, Krumholz LR, Tay ST (2003) Importance of Gram-positive naphthalene-degrading bacteria in oil-contaminated tropical marine sediments. Lett Appl Microbiol 36:251–257

    PubMed  CAS  Google Scholar 

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Acknowledgments

L.D. Sette was supported by grants from CNPq Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil. We thank to PETROBRAS for the financial support and authorization to publish this work, to J.R. Cerqueira for his insightful suggestions, and to Dr. Fernanda F. Piza for the critical reading.

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  1. Microbial Resources Division, CPQBA/UNICAMP, CP 6171, Campinas, SP, CEP 13081-970, Brazil

    Lara D. Sette, Karen C. M. Simioni, Lucia J. Dussan & Valéria M. Oliveira

  2. Chemistry Institute, UNICAMP, CP 6154, Campinas, SP, 13084-971, Brazil

    Suzan P. Vasconcellos & Lucia J. Dussan

  3. PETROBRAS R&D Center, Cidade Universitária, Quadra 7, Ilha do Fundão, Rio de Janeiro, RJ, CEP 21941-598, Brazil

    Eugênio V. S. Neto

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  1. Lara D. Sette
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  2. Karen C. M. Simioni
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  3. Suzan P. Vasconcellos
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  5. Eugênio V. S. Neto
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  6. Valéria M. Oliveira
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Correspondence to Valéria M. Oliveira.

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Sette, L.D., Simioni, K.C.M., Vasconcellos, S.P. et al. Analysis of the composition of bacterial communities in oil reservoirs from a southern offshore Brazilian basin. Antonie van Leeuwenhoek 91, 253–266 (2007). https://doi.org/10.1007/s10482-006-9115-5

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