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Molecular Characterization of an Oil-Degrading Cyanobacterial Consortium

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Abstract

Recent studies have shown that the cyanobacterium Microcoleus chthonoplastes forms a consortium with heterotrophic bacteria present within the cyanobacterial sheath. These studies also show that this consortium is able to grow in the presence of crude oil, degrading aliphatic heterocyclic organo-sulfur compounds as well as alkylated monocyclic and polycyclic aromatic hydrocarbons. In this work, we characterize this oil-degrading consortium through the analysis of the 16S rRNA gene sequences. We performed the study in cultures of Microcoleus grown in mineral medium and in cultures of the cyanobacterium grown in mineral medium supplemented with crude oil. The results indicate that most of the clones found in the polluted culture correspond to well-known oil-degrading and nitrogen-fixing microorganisms, and belong to different phylogenetic groups, such as the Alpha, Beta, and Gamma subclasses of Proteobacteria, and the Cytophaga/Flavobacteria/Bacteroides group. The control is dominated by one predominant organism (88% of the clones) closely affiliated to Pseudoxanthomonas mexicana (similarity of 99.8%). The presence of organisms closely related to well-known nitrogen fixers such as Rhizobium and Agrobacterium suggests that at least some of the cyanobacteria-associated heterotrophic bacteria are responsible for nitrogen fixation and degradation of hydrocarbon compounds inside the polysaccharidic sheath, whereas Microcoleus provides a habitat and a source of oxygen and organic matter.

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References

  1. RMM Abed J Köster (2005) ArticleTitleThe direct role of aerobic heterotrophic bacteria associated with cyanobacteria in the degradation of oil compounds Int Biodeterior Biodegrad 55 29–37 Occurrence Handle1:CAS:528:DC%2BD2MXmslGrsA%3D%3D Occurrence Handle10.1016/j.ibiod.2004.07.001

    Article  CAS  Google Scholar 

  2. RMM Abed NMD Safi J Köster D Beer Particlede Y El-Nahhal J Rullkötter F Garcia-Pichel (2002) ArticleTitleMicrobial diversity of a heavily polluted microbial mat and its community changes following degradation of petroleum compounds Appl Environ Microbiol 68 1674–1683 Occurrence Handle11916684 Occurrence Handle10.1128/AEM.68.4.1674-1683.2002 Occurrence Handle1:CAS:528:DC%2BD38XivFGlt7c%3D

    Article  PubMed  CAS  Google Scholar 

  3. MD Aitken WT Stringfellow RD Nagel C Kazunga SH Chen (1998) ArticleTitleCharacteristics of phenanthrene-degrading bacteria isolated from soils contaminated with polycyclic aromatic hydrocarbons Can J Microbiol 44 743–752 Occurrence Handle9830104 Occurrence Handle10.1139/cjm-44-8-743 Occurrence Handle1:CAS:528:DyaK1cXntleksbc%3D

    Article  PubMed  CAS  Google Scholar 

  4. RH Al-Hasan NA Sorkhoh DA Al-Bader SS Radwan (1994) ArticleTitleUtilization of hydrocarbon by cyanobacteria from microbial mats on oily coasts of the Gulf Appl Microbiol Biotechnol 41 615–619 Occurrence Handle1:CAS:528:DyaK2cXls1emsr8%3D

    CAS  Google Scholar 

  5. RH Al-Hasan DA Al-Bader NA Sorkhoh SS Radwan (1998) ArticleTitleEvidence for n-alkane consumption and oxidation by filamentous cyanobacteria from oil-contaminated coasts of the Arabian Gulf Mar Biol 130 521–527 Occurrence Handle10.1007/s002270050272 Occurrence Handle1:CAS:528:DyaK1cXitVGks7o%3D

    Article  CAS  Google Scholar 

  6. RH Al-Hasan M Khanafer M Eliyas SS Radwan (2001) ArticleTitleHydrocarbon accumulation by picocyanobacteria from the Arabian Gulf J Appl Microbiol 91 533–540 Occurrence Handle11556921 Occurrence Handle10.1046/j.1365-2672.2001.01414.x Occurrence Handle1:CAS:528:DC%2BD3MXmvFKktrw%3D

    Article  PubMed  CAS  Google Scholar 

  7. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller W Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D

    Article  PubMed  CAS  Google Scholar 

  8. EO Casamayor H Schäfer Ll Bañeras C Pedrós-Alió G Muyzer (2000) ArticleTitleIdentification of and spatio-temporal differences between microbial assemblages from two neighboring sulphurous lakes. Comparison by microscopy and denaturing gel electrophoresis Appl Environ Microbiol 66 499–508 Occurrence Handle10653710 Occurrence Handle10.1128/AEM.66.2.499-508.2000 Occurrence Handle1:CAS:528:DC%2BD3cXhtFerur0%3D

    Article  PubMed  CAS  Google Scholar 

  9. CE Cerniglia C Baalen ParticleVan DT Gibson (1980) ArticleTitleMetabolism of naphthalene by the cyanobacterium Oscillatoria sp., strain JCM J Gen Microbiol 116 485–494 Occurrence Handle1:CAS:528:DyaL3cXktVemtbY%3D

    CAS  Google Scholar 

  10. CE Cerniglia C Baalen ParticleVan DT Gibson (1980) ArticleTitleOxidation of byphenyl by the cyanobacterium Oscillatoria sp., strain JCM Arch Microbiol 125 203–207 Occurrence Handle6769418 Occurrence Handle10.1007/BF00446877 Occurrence Handle1:CAS:528:DyaL3cXitFWmtL8%3D

    Article  PubMed  CAS  Google Scholar 

  11. E Dangmann A Stolz AE Kuhm A Hammer B Feigel N Noisommit-Rizzi M Rizzi M Reuss HJ Knackmamss (1996) ArticleTitleDegradation of 4-aminobenzenesulfonate by a two-species bacterial coculture. Physiological interactions between Hydrogenphaga palleronii S1 and Agrobacterium radiobacter S2 Biodegradation 7 223–229 Occurrence Handle8782393 Occurrence Handle10.1007/BF00058181 Occurrence Handle1:CAS:528:DyaK28XntlGqtL0%3D

    Article  PubMed  CAS  Google Scholar 

  12. N Desnoues M Lin X Guo L Ma R Carreño-López C Elmerich (2003) ArticleTitleNitrogen fixation genetics and regulation in a Pseudomonas stutzeri strain associated with rice Microbiology 149 2251–2262 Occurrence Handle12904565 Occurrence Handle10.1099/mic.0.26270-0 Occurrence Handle1:CAS:528:DC%2BD3sXmslaqtrg%3D

    Article  PubMed  CAS  Google Scholar 

  13. Diestra, E, Solé, A, Martí, M, Garcia de Oteyza, T, Grimalt, JO, Esteve, I (2005) Characterization of an oil-degrading Microcoleus consortium by means of CLSM, SEM and TEM. Scanning 27 (in press)

  14. R Eckford FD Cook D Saul J Aislabie J Foght (2002) ArticleTitleFree-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated Antarctic soils Appl Environ Microbiol 68 5181–5185 Occurrence Handle12324373 Occurrence Handle10.1128/AEM.68.10.5181-5185.2002 Occurrence Handle1:CAS:528:DC%2BD38XnvFCks78%3D

    Article  PubMed  CAS  Google Scholar 

  15. JM Foght WS Westlake (1998) ArticleTitleDegradation of polycyclic aromatic hydrocarbons and aromatic heterocycles by a Pseudomonas species Can J Microbiol 34 1135–1141

    Google Scholar 

  16. T Garcia De Oteyza JO Grimalt E Diestra T Solé I Esteve (2004) ArticleTitleChanges in the composition of the polar and apolar crude oil fractions under the action of Microcoleus consortia Appl Microbiol Biotechnol 66 226–232

    Google Scholar 

  17. S Grötzschel J Köster RMM Abed D Beer Particlede (2002) ArticleTitleDegradation of petroleum model compounds immobilized on clay by a hypersaline microbial mat Biodegradation 13 273–283 Occurrence Handle12521291

    PubMed  Google Scholar 

  18. M Harry B Gambier Y Bourezgui E Garnier-Sillam (1999) ArticleTitleEvaluation of purification procedures for DNA extracted from organic samples: interferences with humic substances Analysis 27 439–442 Occurrence Handle1:CAS:528:DyaK1MXmtlOrtrY%3D

    CAS  Google Scholar 

  19. M Lebkowska E Karwowska E Miaskiewicz (1995) ArticleTitleIsolation and identification of bacteria from petroleum derivatives contaminated soil Acta Microbiol Pol 44 297–303 Occurrence Handle8934669 Occurrence Handle1:STN:280:ByiD1cfns1U%3D

    PubMed  CAS  Google Scholar 

  20. W Ludwig O Strunk S Klugbauer N Klugbauer M Weizenegger M Neumaier M Bachleitner KH Schleifer (1998) ArticleTitleBacterial phylogeny based on comparative sequence analysis Electrophoresis 19 554–568 Occurrence Handle9588802 Occurrence Handle10.1002/elps.1150190416 Occurrence Handle1:CAS:528:DyaK1cXisVentrY%3D

    Article  PubMed  CAS  Google Scholar 

  21. MT Madigan DO Jung SM Resnick (2001) ArticleTitleGrowth of the purple bacterium Rhodobacter capsulatus on the aromatic compound hippurate Arch Microbiol 175 462–465 Occurrence Handle11491088 Occurrence Handle10.1007/s002030100284 Occurrence Handle1:CAS:528:DC%2BD3MXltlaqtLs%3D

    Article  PubMed  CAS  Google Scholar 

  22. BL Maidak JR Cole TG Lilburn CT Parker ParticleJr. PR Saxman JM Stredwick GM Garrity B Li GJ Olsen S Pramanik TM Schmidt JM Tiedje (2000) ArticleTitleThe RDP (Ribosomal Database project) continues Nucleic Acids Res 28 73–174 Occurrence Handle10.1093/nar/28.1.173

    Article  Google Scholar 

  23. R Margesin D Labbé F Schinner CW Greer LG Whyte (2003) ArticleTitleCharacterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils Appl Environ Microbiol 69 3085–3092 Occurrence Handle12788702 Occurrence Handle10.1128/AEM.69.6.3085-3092.2003 Occurrence Handle1:CAS:528:DC%2BD3sXks1Glsb0%3D

    Article  PubMed  CAS  Google Scholar 

  24. R Massana AE Murray M Preston EF DeLong (1997) ArticleTitleVertical distribution and phylogenetic characterization of marine planktonic Archaea in the Santa Barbara Channel Appl Environ Microbiol 63 50–56 Occurrence Handle8979338 Occurrence Handle1:CAS:528:DyaK2sXhs1KqtQ%3D%3D

    PubMed  CAS  Google Scholar 

  25. R Muñoz B Guieysse B Mattiasson (2003) ArticleTitlePhenanthrene biodegradation by an algal–bacterial consortium in two-phase partitioning bioreactors Appl Microbiol Biotechnol 61 261–267 Occurrence Handle12698286

    PubMed  Google Scholar 

  26. G Muyzer T Brinkhoff U Nübel C Santegoeds H Schäfer C Wawer (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology ADL Akkermans JD Elsas Particlevan FJ Bruijn (Eds) Molecular Microbial Ecology Manual Kluwer Academic Publishers Dordrecht, The Netherlands

    Google Scholar 

  27. ML Narro CE Cerniglia C Baalen ParticleVan DT Gibson (1992) ArticleTitleMetabolism of phenanthrene by the marine cyanobacterium Agmenellum quadruplicatum PR-6 Appl Environ Microbiol 58 1351–1359 Occurrence Handle1599252 Occurrence Handle1:CAS:528:DyaK38XitFSqt74%3D

    PubMed  CAS  Google Scholar 

  28. JB Olson TF Steppe RW Litaker HW Paerl (1998) ArticleTitleN2-fixing microbial consortia associated with the Ice Cover of Lake Bonney, Antarctica Microb Ecol 36 231–238 Occurrence Handle9852503 Occurrence Handle10.1007/s002489900110 Occurrence Handle1:CAS:528:DyaK1MXks1CktA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  29. HW Paerl JL Pinckney (1996) ArticleTitleA mini-review of microbial consortia: their roles in aquatic production and biogeochemical cycling Microb Ecol 31 225–247 Occurrence Handle8661534 Occurrence Handle10.1007/BF00171569

    Article  PubMed  Google Scholar 

  30. N Palleroni (1993) ArticleTitle Pseudomonas classification Antonie Van Leeuwenhoek 64 231–251 Occurrence Handle8085787

    PubMed  Google Scholar 

  31. MT Prantera A Drozdowicz S Gomes-Leite A Soares-Rosado (2002) ArticleTitleDegradation of gasoline aromatic hydrocarbons by two N2-fixing soil bacteria Biotechnol Lett 24 85–89 Occurrence Handle10.1023/A:1013875431825 Occurrence Handle1:CAS:528:DC%2BD38XhtlKmsbw%3D

    Article  CAS  Google Scholar 

  32. C Raghukumar V Vipparty JJ David D Chandramohan (2001) ArticleTitleDegradation of crude oil by cyanobacteria Appl Microbiol Biotechnol 57 433–436 Occurrence Handle11759698 Occurrence Handle1:CAS:528:DC%2BD3MXotlahtb0%3D

    PubMed  CAS  Google Scholar 

  33. L Raskin JM Stromley BE Rittmann DA Stahl (1994) ArticleTitleGroup-specific 16S rRNA hybridization probes to describe natural communities of methanogens Appl Environ Microbiol 60 1232–1240 Occurrence Handle7517128 Occurrence Handle1:CAS:528:DyaK2cXkt1yjt70%3D

    PubMed  CAS  Google Scholar 

  34. K Ravenschlag K Sahm J Pernthaler R Amann (1999) ArticleTitleHigh bacterial diversity in permanently cold marine sediments Appl Environ Microbiol 65 3982–3989 Occurrence Handle10473405 Occurrence Handle1:CAS:528:DyaK1MXlvFeqtbs%3D

    PubMed  CAS  Google Scholar 

  35. M Schauer R Massana C Pedrós-Alió (2000) ArticleTitleSpatial differences in bacterioplankton composition along the Catalan coast (NW Mediterranean) assessed by molecular fingerprinting FEMS Microbiol Ecol 33 51–59 Occurrence Handle10922503 Occurrence Handle1:CAS:528:DC%2BD3cXltVOmtbs%3D

    PubMed  CAS  Google Scholar 

  36. D Schleheck BJ Tindall R Rossello-Mora AM Cook (2004) ArticleTitle Parvivaculum lavamentivorans gen. nov., sp. nov., a novel heterotroph that initiates catabolism of linear alkylbenzenesulfonate Int J Syst Evol Microbiol 54 1489–1497 Occurrence Handle15388700 Occurrence Handle1:CAS:528:DC%2BD2cXptVOls7Y%3D

    PubMed  CAS  Google Scholar 

  37. DA Stahl RI Amann (1991) Development and application of nucleic acid probes E Stackebrandt M Goodfellow (Eds) Nucleic Acid Techniques in Bacterial Systematics Wiley New York, NY 205–248

    Google Scholar 

  38. TF Steppe JB Olson HW Paerl RW Litaker J Belnap (1996) ArticleTitleConsortial N2 fixation: a strategy for meeting nitrogen requirements of marine and terrestrial cyanobacterial mats FEMS Microbiol Ecol 21 149–156 Occurrence Handle1:CAS:528:DyaK28XmsVynsr0%3D

    CAS  Google Scholar 

  39. NA Sorkhoh R Al-Hasan S Radwan T Hopner (1992) ArticleTitleSelf-cleaning of the Gulf Nature 359 109 Occurrence Handle10.1038/359109a0

    Article  Google Scholar 

  40. L Suominen MM Jussila K Mäkeläinen M Romantschuk K Lindström (2000) ArticleTitleEvaluation of the Galega–Rhizobium galegae system for the bioremediation of oil-contaminated soil Environ Pollut 107 239–244 Occurrence Handle15093001 Occurrence Handle10.1016/S0269-7491(99)00143-8 Occurrence Handle1:CAS:528:DC%2BD3cXhslSnsr8%3D

    Article  PubMed  CAS  Google Scholar 

  41. S Thierry H Macarie T Iizuka W Geissdorfer EA Assih M Spanevello F Verhe P Thomas R Fudou O Monroy M Labat M Ouattara (2004) ArticleTitle Pseudoxanthomonas mexicana sp. nov, and Pseudoxanthomonas japonensis sp. nov., isolated from diverse environments, and emended descriptions of the genus Pseudoxanthomonas Finkmann et al. 2000 and of its type species Int J Syst Evol Microbiol 54 2245–2255 Occurrence Handle15545466 Occurrence Handle1:CAS:528:DC%2BD2cXhtFGjsL%2FJ Occurrence Handle10.1099/ijs.0.02810-0

    Article  PubMed  CAS  Google Scholar 

  42. H Gemerden ParticleVan HH Beeftink (1983) Ecology of phototrophic bacteria JG Ormerod (Eds) The Phototrophic Bacteria: Anaerobic Life in the Light Blackwell Scientific Publications Oxford 146–185

    Google Scholar 

  43. H Zhang A Kallimanis AI Koukhou C Drainas (2004) ArticleTitleIsolation and characterization of novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils Appl Microbiol Biotechnol 65 124–131 Occurrence Handle15133642 Occurrence Handle10.1007/s00253-004-1614-6 Occurrence Handle1:CAS:528:DC%2BD2cXkvF2murc%3D

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants BOS2000-0139, REN2000-0332-P4 and DPI2003-0860-C03-02 from the Ministerio de Ciencia y Tecnología to J Mas.

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  1. Departament de Genètica i Microbiologia, Facultat de Ciències, Universitat Autònoma de Barcelona, 08193, Bellaterra, Spain

    Olga Sánchez, Elia Diestra, Isabel Esteve & Jordi Mas

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  1. Olga Sánchez
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  2. Elia Diestra
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  3. Isabel Esteve
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Correspondence to Olga Sánchez.

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Sánchez, O., Diestra, E., Esteve, I. et al. Molecular Characterization of an Oil-Degrading Cyanobacterial Consortium. Microb Ecol 50, 580–588 (2005). https://doi.org/10.1007/s00248-005-5061-4

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