Skip to main content

Advertisement

Log in

Biofilm comprising phototrophic, diazotrophic, and hydrocarbon-utilizing bacteria: a promising consortium in the bioremediation of aquatic hydrocarbon pollutants

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Biofilms harboring simultaneously anoxygenic and oxygenic phototrophic bacteria, diazotrophic bacteria, and hydrocarbon-utilizing bacteria were established on glass slides suspended in pristine and oily seawater. Via denaturing gradient gel electrophoresis analysis on PCR-amplified rRNA gene sequence fragments from the extracted DNA from biofilms, followed by band amplification, biofilm composition was determined. The biofilms contained anoxygenic phototrophs belonging to alphaproteobacteria; pico- and filamentous cyanobacteria (oxygenic phototrophs); two species of the diazotroph Azospirillum; and two hydrocarbon-utilizing gammaproteobacterial genera, Cycloclasticus and Oleibacter. The coexistence of all these microbial taxa with different physiologies in the biofilm makes the whole community nutritionally self-sufficient and adequately aerated, a condition quite suitable for the microbial biodegradation of aquatic pollutant hydrocarbons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Al-Awadhi H, Al-Hasan RH, Sorkhoh NA, Salamah S, Radwan SS (2003) Establishing oil-degrading biofilms on gravel particles and glass plates. Int Biodeter Biodeg 51:181–185

    Article  CAS  Google Scholar 

  • Al-Awadhi H, Al-Mailem D, Dashti, Khanafer M, Radwan SS (2012) Indigenous hydrocarbon-utilizing bacterioflora in oil-polluted habitats in Kuwait, two decades after the greatest man-made oil spill. Arch Microbiol 194:689–705

    Article  CAS  Google Scholar 

  • Al-Bader D, Eliyas M, Rayan R, Radwa SS (2012) Air–dust-borne associations of phototrophic and hydrocarbon-utilizing microorganisms: promising consortia in volatile hydrocarbon bioremediation. Environ Sci Pollut Res 19:3997–4005

    Article  CAS  Google Scholar 

  • Al-Hasan RH, Khanafer M, Eliyas M, Radwan SS (2001) Hydrocarbon accumulation by picocyanobacteria from the Arabian Gulf. J Appl Microbiol 91:533–540

    Article  CAS  Google Scholar 

  • Ali N, Dashti N, Al-Mailem D, Eliyas M, Radwan S (2012) Indigenous soil bacteria with the combined potential for hydrocarbon-consumption and heavy-metal-resistance. Environ Sci Pollut Res 19:812–820

    Article  CAS  Google Scholar 

  • Canfield DE, Des Marais DJ (1993) Biogeochemical cycles of carbon, sulfur, and free oxygen in a microbial mat. Geochim Cosmochim Acta 57:3971–3984

    Article  CAS  Google Scholar 

  • Chan BK, Chan WK, Walker G (2003) Patterns of biofilm succession on a sheltered rocky shore in Hong Kong. Biofouling 19:371–380

    Article  Google Scholar 

  • Chandran P, Das N (2011) Degradation of diesel oil by immobilized Candida tropicalis and biofilm formed on gravel. Biodegradation 22:1181–1189

    Article  CAS  Google Scholar 

  • Chung WK, King GM (2001) Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen. nov., sp. nov. and Cycloclasticus spirillensus sp. nov. Appl Environ Microb 67:5585–5592

    Article  CAS  Google Scholar 

  • Costerton JW, Stewart PS (1999) Greenberg EP bacterial biofilms: a common cause of persistent infections. Science 284:1318–1320

    Article  CAS  Google Scholar 

  • Dahllöf I, Baillie H, Kjelleberg S (2000) rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Appl Environ Microbiol 66:3376–3380

    Article  Google Scholar 

  • Eckford R, Cook F, Saul D, Aislabie J, Foght J (2002) Free-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated Antarctic soil. Appl Environ Microbiol 68:5181–5185

    Article  CAS  Google Scholar 

  • Golby S, Ceri H, Gieg LM, Chatterjee I, Margues LL, Turner RJ (2012) Evaluation of microbial biofilm communities from an Alberta oil sands tailings pond. FEMS Microbial Ecol 79:240–250

    Article  CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    Article  CAS  Google Scholar 

  • Jarvi HP, Neal C, Warwick A, White J, Neal M, Wickham HD, Hill LK, Andrews MC (2002) Phosphorus uptake into algal biofilms in a lowland chalk river. Sci Total Environ 282–283:353–373

    Article  Google Scholar 

  • Klug J, Markovetz J (1971) Utilization of aliphatic hydrocarbons by micro-organisms. Adv Microb Physiol 5:1–39

    Article  CAS  Google Scholar 

  • Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54(3):305–315

    CAS  Google Scholar 

  • Nadell CD, Xavier JB, Foster KR (2009) The sociobiology of biofilms. FEMS Mirobiol Rev 33:206–224

    Article  CAS  Google Scholar 

  • Nübel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microb 63:3327–3332

    Google Scholar 

  • Ortega-Morales O, Guezennec J, Hernandez-Duque G, Gaylarde CC, Gaylarde PM (2000) Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Curr Microbiol 40:81–85

    Article  CAS  Google Scholar 

  • Paerl HW, Pinckney JL, Steppe TF (2000) Cyanobacterial–bacterial mat consortia: examining the functional unit of microbial survival and growth in extreme environments. Environ Microbiol 2:11–26

    Article  CAS  Google Scholar 

  • Puente M, Holguin G, Glick B, Bashan Y (1999) Root-surface colonization of black mangrove seedlings by Azospirillum halopraeferens and Azospirillum brasilense in seawater. FEMS Mirobiol Ecol 29:283–292

    Article  CAS  Google Scholar 

  • Radwan SS, Al-Hasan RH, Salamah S, Khanafer M (2005) Oil-consuming microbial consortia floating in the Arabian Gulf. Int Biodeter Biodeg 56:28–33

    Article  CAS  Google Scholar 

  • Radwan SS, Al-Hasan RH (2001a) Potential application of coastal biolfilm-coated gravel particles for treating oily waste. Aqu Microb Ecol 23:113–117

    Article  Google Scholar 

  • Radwan SS, Al-Hasan RH (2001b) Cyanobacteria and the Self-Cleaning of oily Environments. In: Kojima H, Lee YK (eds) Photosynthetic microorganisms in Environmental Biotechnology. Chapter 12. Springer, New York, pp 181–193

    Google Scholar 

  • Radwan SS, Al-Hasan RH, Salamah S, Al-Dabbous S (2002) Bioremediation of oily sea water by bacteria immobilized in biofilms coating macroalgae. Int Biodeter Biodeg 50:55–59

    Article  CAS  Google Scholar 

  • Radwan SS, Al-Mailem D, El-Nemr I, Salamah S (2000) Enhanced remediation of hydrocarbon contaminated desert soil fertilized with organic carbon. Int Biodeter Biodeg 46:129–132

    Article  CAS  Google Scholar 

  • Radwan SS, Mahmoud H, Khanafer M, Al-Habib A, Al-Hasan R (2010) Identities of epilithic hydrocarbon-utilizing diazotrophic bacteria from the Arabian Gulf coasts, and their potential for oil bioremediation without nitrogen supplementation. Microbiol Ecol 60:354–363

    Article  CAS  Google Scholar 

  • Ravikumar S, Ramanathan G, Suba N, Jeyaseeli L (2002) Quantification of halophilic Azospirillum from mangroves. Ind J Mar Sci 31(2):157–160

    Google Scholar 

  • Rhem HJ, Reiff J (1981) Mechanisms and occurrence of microbial oxidation of long-chain alkanes. Adv Biochem Eng 19:175–215

    Google Scholar 

  • Rippka RJ, Deruelles JB, Waterbury M, Herdman RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Appl Microbiol 111:1–61

    Google Scholar 

  • Roeselers G, Loosdrecht MCM, Muyzer G (2007) Heterotrophic pioneers facilitate biofilm development. Microbial Ecol 54:578–585

    Article  CAS  Google Scholar 

  • Schäfer H, Muyzer G (2001) Denaturing gradient gel electrophoresis in marine microbial ecology. Methods in Microbiology 30:425–468

    Article  Google Scholar 

  • Schumacher G, Blume T, Sekoulov I (2003) Bacteria reduction and nutrient removal in small wastewater treatment plants by an algal biofilm. Water Sci Technol 47:195–202

    CAS  Google Scholar 

  • Sekiguchi H, Tomioka N, Nakahara T, Uchiyama H (2001) A single band does not always represent single bacterial strains in denaturing gradient gel electrophoresis analysis. Biotechnol Lett 23:1205–1208

    Article  CAS  Google Scholar 

  • Sorkhoh N, Al-Hasan R, Radwan S, Höpner T (1992) Self-cleaning of the Gulf. Nature 350:109

    Article  Google Scholar 

  • Sorkhoh NA, Ali N, Dashti N, Al-Mailem DM, Eliyas M, Radwan SS (2010a) Soil bacteria with the combined potential for oil-utilization, nitrogen-fixation and mercury-resistance. Int Biodeter Biodegr 64:226–231

    Article  CAS  Google Scholar 

  • Sorkhoh NA, Ali N, Salamah S, Eliyas M, Khanafer M, Radwan SS (2010b) Enrichment of rhizospheres of crop plants raised in oily sand with hydrocarbon utilizing bacteria capable of hydrocarbon consumption in nitrogen free media. Int Biodeter Biodegr 64:659–664

    Article  CAS  Google Scholar 

  • Stal LJ, Krukbein E (1985) Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp. Arch Microbiol 143:72–76

    Article  CAS  Google Scholar 

  • Teramoto M, Ohuchi M, Hatmanti A, Darmayati Y, Widyastuti Y, Harayama S, Fukunaga Y (2011) Oleibacter marinus gen. nov., sp. nov., a bacterium that degrades petroleum aliphatic hydrocarbons in a tropical marine environment. Int J Syst Evol Microbiol 61:375–380

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Vaysse PJ, Sivadon P, Goulas P, Grimaud R (2011) Cells dispersed from Marinobacter hydrocarbonocasticus SP17 biofilm exhibit a specific protein profile associated with a higher ability to reinitiate biofilm development at the hexadecane–water interface. Environ Microbiol 13:737–746

    Article  CAS  Google Scholar 

  • Vymazal J, Sladedek V, Stach J (2001) Biota participating in wastewater treatment in a horizontal flow constructed wetland. Water Sci Technol 44:211–214

    CAS  Google Scholar 

  • Wyatt JT, Silvey JKG (1969) Nitrogen fixation by Gloeocapsa. Science 165:908–909

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work has been supported by the Kuwait University, research grant SL02/08. We would also like to acknowledge the use of ABI 3130xl Genetic Analyzer under the General Facility Projects GS01/02 and Mrs. Leena Idicula for her technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Samir S. Radwan.

Additional information

Responsible editor: Robert Duran

Rights and permissions

Reprints and permissions

About this article

Cite this article

Al-Bader, D., Kansour, M.K., Rayan, R. et al. Biofilm comprising phototrophic, diazotrophic, and hydrocarbon-utilizing bacteria: a promising consortium in the bioremediation of aquatic hydrocarbon pollutants. Environ Sci Pollut Res 20, 3252–3262 (2013). https://doi.org/10.1007/s11356-012-1251-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-012-1251-z

Keywords

Navigation