Advertisement

Microbial Consortia and Biodegradation of Petroleum Hydrocarbons in Marine Environments

  • J. Paniagua-MichelEmail author
  • Babu Z. Fathepure
Chapter

Abstract

The pollution of petroleum hydrocarbons in the sea is an increasingly widespread international problem that threatens the environment and human health. At present, there are important advances in relation to innovative and effective technologies for the elimination of oil contaminants from the marine environment. The main advantages of microbial remediation lie in its low cost and high efficiency in a sustainable manner. Numerous laboratory-scale studies and field application of microorganisms to clean up hydrocarbon-impacted marine and coastal environments have clearly demonstrated the viability of bioremediation technologies under various environmental conditions. In addition, due to the complex mixture represented by petroleum hydrocarbons, a consortium of taxonomically diverse species with broad enzymatic capabilities is required, because a single species can metabolize only a limited range of hydrocarbon substrates. Because, in natural environments, most of the microorganisms (>99%) coexist in the form of microbial consortia, there are major expectations on the uses of consortia of microorganisms to perform the degradation of complex molecules present in petroleum hydrocarbons. The members of the microbial communities acting together may exhibit the ability to secrete biosurfactants leading to the enhanced solubilization and removal of hydrophobic hydrocarbons. Recent reports have evidenced that halophilic bacteria and archaea have the capacity not only to cope with high-salinity stress but also be able to metabolize n-alkanes and PAHs suggesting their key role in mitigating vast areas of highly saline coastal habitats impacted by petroleum compounds that pose threat to both terrestrial and marine ecosystems. In this chapter, we report on recent developments on the biodegradation and bioremediation of petroleum hydrocarbons by microbial communities in marine and other high-salinity environments, and molecular mechanism of hydrocarbon degradation in halophiles has been described.

References

  1. Abed RM, Al-Thukair A, De Beer D (2006) Bacterial diversity of a cyanobacterial mat degrading petroleum compounds at elevated salinities and temperatures. FEMS Microbiol Ecol 57:290–301CrossRefGoogle Scholar
  2. Atlas R, Bragg J (2009) Bioremediation of marine oil spills: when and when not–the Exxon Valdez experience. Microb Biotechnol 2:213–221Google Scholar
  3. Al-Hasan RH, Al-Bader DA, Sorkhoh NA, Radwan SS (1998) Evidence for n -alkane consumption and oxidation by filamentous cyanobacteria from oil-contaminated coasts of the Arabian Gulf. Mar Biol 130(3):521–527CrossRefGoogle Scholar
  4. Al-Mailem DM, Sorkhoh NA, Al-Awadhi H, Eliyas M, Radwan SS (2010) Biodegradation of crude oil and pure hydrocarbons by extreme halophilic archaea from hypersaline coasts of the Arabian Gulf. Extremophiles 14:321–328CrossRefGoogle Scholar
  5. Al-Mailem DM, Eliyas M, Radwan SS (2013) Oil-bioremediation potential of two hydrocarbonoclastic, diazotrophic Marinobacter strains from hypersaline areas along the Arabian Gulf coasts. Extremophiles 17:463–470CrossRefGoogle Scholar
  6. Al-Mueini R, Al-Dalali M, Al-Amri IS, Patzelt H (2007) Hydrocarbon degradation at high salinity by a novel extremely halophilic actinomycete. Environ Chem 4:5–7CrossRefGoogle Scholar
  7. Banat IM, Satpute SK, Cameotra SS, Patil R, Nyayanit NV (2014) Cost effective technologies and renewable substrates for biosurfactants’ production. Front Microbiol 5(5):697.  https://doi.org/10.3389/fmicb.2014.00697
  8. Bao M, Wanga L, Sun P, Cao L, Zou J, Li Y (2012) Biodegradation of crude oil using an efficient microbial consortium in a simulated marine environment. Mar Pollut Bull 64:1177–1185CrossRefGoogle Scholar
  9. Bertrand J-C, Almallah M, Acquaviva M, Mille G (1990) Biodegradation of hydrocarbons by an extremely halophilic archaebacterium. Lett Appl Microbiol 11:260–263CrossRefGoogle Scholar
  10. Bonfá MRL, Grossman MJ, Mellado E, Durrant LR (2011) Biodegradation of aromatic hydrocarbons by Haloarchaea and their use for the reduction of the chemical oxygen demand of hypersaline petroleum produced water. Chemosphere 84:1671–1676CrossRefGoogle Scholar
  11. Brenner K, Lingchong Y, Frances HA (2008) Engineering microbial consortia: a new frontier in synthetic biology. Trends Biotechnol 26(9):483–489CrossRefGoogle Scholar
  12. Burmolle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S (2006) Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916–3923CrossRefGoogle Scholar
  13. Cao B, Nagarajan K, Loh KC (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85(2):207–228CrossRefGoogle Scholar
  14. Castillo-Carvajal LC, Sanz-Martín JL, Barragán-Huerta BE (2014) Biodegradation of organic pollutants in saline wastewater by halophilic microorganisms: a review. Environ Sci Pollut Res 21:9578–9588CrossRefGoogle Scholar
  15. Cerniglia CE, Gibson DT, Van Baalen C (1980) Oxidation of naphthalene by cyanobacteria and microalgae. J Gen Microbiol 116:495–500Google Scholar
  16. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368CrossRefGoogle Scholar
  17. Chronopoulou, Sanni GO, Silas-Olu DI, van der Meer JR, Timmis KN, Brussaard CPD, McGenity TJ (2014) Generalist hydrocarbon-degrading bacterial communities in the oil-polluted water column of the North Sea. Microbial Biotechnol 8(3):434:447Google Scholar
  18. Coulon F, Chronopoulou P-M, Fahy A, Païssé S, Goñi-Urriza M, Peperzak L, Alvarez LA, McKew BA, Brussaard CPD, Underwood GJC, Timmis KN, Duran R, McGenity TJ (2012) Central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms in the biodegradation of hydrocarbons in coastal mudflats. Appl Environ Microbiol 78(10):3638–3648CrossRefGoogle Scholar
  19. Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int. Article ID 941810, 13 pages.  https://doi.org/10.4061/2011/941810 Google Scholar
  20. Dastgheib SMM, Amoozegar MA, Khajeh K, Ventosa A (2011) A halotolerant Alcanivorax sp. strain with potential application in saline soil remediation. Appl Microbiol Biotechnol 90:305–312CrossRefGoogle Scholar
  21. Dastgheib SMM, Amoozegar MA, Khajeh K, Shavandi M, Ventosa A (2012) Biodegradation of polycyclic aromatic hydrocarbons by a halophilic microbial consortium. Appl Microbiol Biotechnol 95:789–798CrossRefGoogle Scholar
  22. Deppe U, Richnow HH, Michaelis W, Antranikian G (2005) Degradation of crude oil by an arctic microbial consortium. Extremophiles 9:461–470CrossRefGoogle Scholar
  23. Ding MZ, Song H, Wang EX, Liu Y, Yuan YJ (2016) Design and construction of synthetic microbial consortia in China. Synth Syst Biotechnol 1:230–235CrossRefGoogle Scholar
  24. Divya M, Aanand S, Srinivasan A, Ahilan B (2015) Bioremediation-an eco-friendly tool for effluent treatment: a review. Int J Appl Res 1(12):530–537Google Scholar
  25. Erdogmuş SF, Mutlu B, Korcan SE, Guven K, Konuk M (2013) Aromatic hydrocarbon degradation by halophilic archaea isolated from Çamaltı Saltern, Turkey. Water Air Soil Pollut 224:1449–1454CrossRefGoogle Scholar
  26. Fathepure BZ (2014) Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments. Front Microbiol 5.  https://doi.org/10.3389/fmicb.2014.00173
  27. Fernandez-Linares L, Acquaviva M, Bertrand JC, Gauthier M (1996) Effect of sodium chloride concentration on growth and degradation of eicosane by the marine halotolerant bacterium Marinobacter hydrocarbonoclasticus. Syst Appl Microbiol 19:113–121CrossRefGoogle Scholar
  28. Gao W, Cui Z, Li Q, Xu G, Jia X, Zheng L (2013) Marinobacter nanhaiticus sp. nov., polycyclic aromatic hydrocarbon-degrading bacterium isolated from the sediment of the South China Sea. Antonie Van Leeuwenhoek 103:485–491CrossRefGoogle Scholar
  29. 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
  30. Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369.  https://doi.org/10.3389/fmicb.2016.01369 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gibbs GW (1997) Estimating residential polycyclic aromatic hydrocarbon (PAH) related lung cancer risk using occupational data. Ann Occup Hyg 41:49–53Google Scholar
  32. Gomes MB, Gonzales-Limache EE, Sousa STP, Dellagnezze BM, Sartoratto A, Silva LCF, Gieg LM, Valoni E, Souza RS, Torres APR, Sousa MP, De Paula SO, Silva CC, Oliveira VM (2016) Exploring the potential of halophilic bacteria from oil terminal environments for biosurfactant production and hydrocarbon degradation under high salinity conditions. Int Biodeterior Biodegrad 126:231–242CrossRefGoogle Scholar
  33. Guo G, Fang T, Wang C, Huang Y, Tian F, Cui Q, Wang H (2015) Isolation and characterization of two novel halotolerant catechol 2, 3-dioxygenases from a halophilic bacterial consortium. Sci Rep 5(1):17603.  https://doi.org/10.1038/srep17603 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Harayama S, Kishira H, Kasai Y, Shutsubo K (1999) Petroleum biodegradation in marine environments. J Mol Microbiol Biotechnol 1:63–70PubMedGoogle Scholar
  35. Hassanshahian M, Emtiazi G, Caruso G, Cappello S (2014) Bioremediation (bioaugmentation/biostimulation) trials of oil polluted seawater: a mesocosm simulation study. Mar Environ Res 95:28–38CrossRefGoogle Scholar
  36. 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
  37. Joutey NT, Bahafid W, Sayel H and El Ghachtouli N (2013). Biodegradation: involved microorganisms and genetically engineered microorganisms, biodegradation Rolando Chamy and Francisca Rosenkranz, IntechOpen,  https://doi.org/10.5772/s56194. Available from: https://www.intechopen.com/books/biodegradation-life-ofscience/biodegradation-involved-microorganisms-and-genetically-engineered-microorganisms
  38. Juhasz A, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: A review of the microbial degradation of Benzo[a]pyrene. Int Biodeterior Biodegrad 45(1–2):57–88CrossRefGoogle Scholar
  39. Kanaly RA, Harayama S (2000) Biodegradation of high-molecular weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067CrossRefGoogle Scholar
  40. Khemili Talbi S, Kebbouche Gana S, Akmoussi Toumi S, Angar Y, Gana ML (2015) Isolation of an extremely halophilic arhaeon Natrialba sp. C21 able to degrade aromatic compounds and to produce stable biosurfactant at high salinity. Extremophiles 19:1109–1120CrossRefGoogle Scholar
  41. Kulichevskaya IS, Milekhina EI, Borzenkov IA, Zvyagintseva IS, SS B (1991) Oxidation of petroleum-hydrocarbons by extremely halophilic archaebacteria. Microbiology 60:596–601Google Scholar
  42. Le Borgne S, Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92CrossRefGoogle Scholar
  43. Malik ZA, Ahmed S (2012) Degradation of petroleum hydrocarbons by oil field isolated bacterial consortium. Afr J Biotechnol 11:650–658Google Scholar
  44. Maneerat S (2005) Biosurfactants from marine microorganisms. J Sci Technol 27:1263–1272Google Scholar
  45. Margesin R, Schinner F (2001) Biodegradation and bioremediation of hydrocarbons in extreme environments. Appl Microbiol Biotechnol 56:650–663CrossRefGoogle Scholar
  46. Martins LF, Peixoto RS (2012) Biodegradation of petroleum hydrocarbons in hypersaline environments. Braz J Microbiol 43:865–872CrossRefGoogle Scholar
  47. McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat Biosyst 8(1):10.  https://doi.org/10.1186/2046-9063-8-10 CrossRefGoogle Scholar
  48. McGenity TJ (2014) Hydrocarbon biodegradation in intertidal wetland sediments. Curr Opin Biotechnol 27:46–54CrossRefGoogle Scholar
  49. Menzie CA, Potocki BB, Santodonato J (1992) Exposure to carcinogenic PAH in the environment. Environ Sci Technol 26:1278–1284CrossRefGoogle Scholar
  50. Mnif S, Chamkha M, Sayadi S (2009) Isolation and characterization of Halomonas sp. strain C2SS100, a hydrocarbon-degrading bacterium under hypersaline conditions. J Appl Microbiol 107:785–794CrossRefGoogle Scholar
  51. Mnif S, Chamkha M, Labat M, Sayadi S (2011) Simultaneous hydrocarbon biodegradation and biosurfactant production by oilfield-selected bacteria. J Appl Microbiol 111:525–536CrossRefGoogle Scholar
  52. National Research Council (US) Committee on Oil in the Sea: Inputs, Fates, and Effects (2003) Oil in the sea III: inputs, fates, and effects. National Academies Press, Washington, DCCrossRefGoogle Scholar
  53. Nie Y, Fang H, Li Y, Chi CQ, Tang YQ, Wu XL (2013) The genome of the moderate halophile Amycolicicoccus subflavus DQS3-9A1T reveals four alkane hydroxylation systems and provides some clues on the genetic basis for its adaptation to a petroleum environment. PLoS One 8(8):e70986.  https://doi.org/10.1371/journal.pone.0070986 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Olajire AA, Essien JP (2014) Aerobic degradation of petroleum components by microbial consortia. J Pet Environ Biotechnol 5:5–8CrossRefGoogle Scholar
  55. Oren A (2017) Aerobic hydrocarbon-degradation archaea. Taxonomy, genomics and ecophysiology of hydrocarbon-degrading microbes. In: McGenity TJ (ed) Hydrocarbon and lipid metabolism. Springer International Publishing AG 2017, Berlin HeidelbergGoogle Scholar
  56. Paniagua Michel J, Rosales Morales A (2015) Marine bioremediation – a sustainable biotechnology of petroleum hydrocarbons biodegradation in coastal and marine environments. J Bioremed Biodegr 6:1–6Google Scholar
  57. Paniagua Michel J, Olmos J, Morales Guerrero ER (2014) Algal and microbial exopolysaccharides: new insights as biosurfactants and bioemulsifiers. Adv Food Nutri Res 73:221–257CrossRefGoogle Scholar
  58. Paniagua-Michel J (2017) Wastewater treatment using phototrophic–heterotrophic biofilms and microbial mats. In: Prospects and challenges in algal biotechnology. Springer, Singapore, pp 257–275CrossRefGoogle Scholar
  59. Patowary K, Patowary R, Kalita MC, Deka S (2016) Development of an efficient bacterial consortium for the potential remediation of hydrocarbons from contaminated sites. Front Microbiol 7:1092–1099CrossRefGoogle Scholar
  60. Prince RC (2010) Eukaryotic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology. Springer, Berlin/Heidelberg, pp 2065–2078CrossRefGoogle Scholar
  61. Prince RC, Walters CC (2007) Biodegradation of oil and its implications for source identification. In: Wang Z, Stout SA (eds) Oil spill environmental forensics. Academic Press, Burlington, pp 349–379CrossRefGoogle Scholar
  62. Priya A, Mandal AK, Ball AS, Manefield M, Lal B, Sarma PM (2015) Mass culture strategy for bacterial yeast co-culture for degradation of petroleum hydrocarbons in marine environment. Europe PMC Plus 100(1):191–199Google Scholar
  63. Pugazhendi A, Qari H, Al-Badry Basahi JM, Godon JJ, Dhavamani J (2017) Role of a halothermophilic bacterial consortium for the biodegradation of PAHs and the treatment of petroleum wastewater at extreme conditions. Int Biodeterior Biodegrad 121:44–54CrossRefGoogle Scholar
  64. Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11:2477–2490CrossRefGoogle Scholar
  65. Rosales Morales A, Paniagua Michel J (2014) Bioremediation of hexadecane and diesel oil is enhanced by photosynthetically produced marine biosurfactants. J Bioremed Biodegr 34:1–5Google Scholar
  66. Safonova E, Kvitko KV, Ienkevitch MI, Surgko LF, Afti IA, Reisser W (2004) Biotreatment of industrial waste water by selected algae-bacterial consortia. Eng Life Sci 4:347–353CrossRefGoogle Scholar
  67. Sass AM, McKew BA, Sass H, Fichtel J, Timmis KN, McGenity TJ (2008) Diversity of Bacillus like organisms isolated from deep sea hypersaline anoxic sediments. Saline Syst 4:8–14CrossRefGoogle Scholar
  68. Shen T, Pi Y, Bao M, Xu N, Li Y, Lu J (2017) Biodegradation of different petroleum hydrocarbons by free and immobilized microbial Consortia. Environ Sci Processes Impacts 17:2022–2033CrossRefGoogle Scholar
  69. Snape I, Riddle MJ, Stark JS et al (2001) Management andremediation of contaminated sites at Casey station, Antarctica. Polar Rec 37:199–214CrossRefGoogle Scholar
  70. Sorokin DY, Janssen AJH, Muyzer G (2012) Biodegradation potential of halo (alkali) philic prokaryotes. Crit Rev Environ Sci Technol 42:811–856CrossRefGoogle Scholar
  71. Subashchandrabose SR, Ramakrishnan B, Megharaj M, Venkateswarlu K, Naidu R (2011) Consortia of cyanobacteria/microalgae and bacteria: biotechnological potential. Biotechnol Adv 29:896–907CrossRefGoogle Scholar
  72. Sugiura K, Ishihara M, Shimauchi T et al (1997) Physicochemical properties and biodegradability of crude oil. Environ Sci Technol 31:45–51CrossRefGoogle Scholar
  73. Tapilatu YH, Grossi V, Acquaviva M, Militon C, Bertrand JC, Cuny P (2010) Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France). Extremophiles 14:225–231CrossRefGoogle Scholar
  74. Van Hamme JD, Singh AM, OP W (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 6:503–549CrossRefGoogle Scholar
  75. Wang W, Shao Z (2013) Enzymes and genes involved in aerobic alkane degradation. Front Microbiol 4:116.  https://doi.org/10.3389/fmicb.2013.00116 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang C, Guo G, Huang Y, Hao H, Wang H (2017) Salt adaptation and evolutionary implication of a Nah-related PAHs dioxygenase cloned from a halophilic phenanthrene degrading consortium. Sci Rep 7:12525CrossRefGoogle Scholar
  77. Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hypersaline environments. Appl Environ Microbiol 35:353–359PubMedPubMedCentralGoogle Scholar
  78. Whitehouse BG (1984) The effects of temperature and salinity on the aqueous solubility of polynuclear aromatic hydrocarbons. Mar Chem 14:319–332CrossRefGoogle Scholar
  79. Yakimov MM, Golyshin PN, Lang S, Moore ER, Abraham WR, Lunsdorf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant producing marine bacterium. Int J Syst Bacteriol 48:339–348CrossRefGoogle Scholar
  80. Yakimov MM, Guiliano L, Crisafi E, Chemikova 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
  81. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil degrading marine bacteria. Curr Opin Biotechnol 18:257–266CrossRefGoogle Scholar
  82. Zhao B, Wang H, Mao X, Li R (2009) Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Curr Microbiol 58:205–210CrossRefGoogle Scholar
  83. Zhao D, Kumar S, Zhou J, Wang R, Li M, Xiang H (2017) Isolation and complete genome sequence of Halorientalis hydrocarbonoclasticus sp. nov., a hydrocarbon degrading haloarchaeon. Extremophiles 21:1081–1090CrossRefGoogle Scholar
  84. Zhou H, Wang H, Huang Y, Fang T (2016) Characterization of pyrene degradation by halophilic Thalassospira sp. strain TSL5-1 isolated from the coastal soil of Yellow Sea, China. Int Biodeterior Biodegrad 107:62–69CrossRefGoogle Scholar
  85. Zvyagintseva IS, Poglasova MN, Gotoeva MT, Belyaev SS (2001) Effect of the medium salinity on oil degradation by Nocardioform bacteria. Microbiology 70:652–656CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Marine BiotechnologyCentro de Investigacion Cientifica y de Educacion Superior de Ensenada (CICESE)EnsenadaMexico
  2. 2.Department of Microbiology and Molecular GeneticsOklahoma State UniversityStillwaterUSA

Personalised recommendations