Biosurfactant production from marine hydrocarbon-degrading consortia and pure bacterial strains using crude oil as carbon source

Frontiers in Microbiology

Volumn 6, Issue APR, 2015, Pages

  Antoniou, Eleftheria ^a   Fodelianakis, Stilianos ^a   Korkakaki, Emmanouela ^a   Kalogerakis, Nicolas ^a  

^a TECHNICAL UNIVERSITY OF CRETE   (Greece)

Author keywords

Alcanivorax; Bioaugmentation; Biosurfactant; Crude oil; Marine bacteria; Paracoccus marcusii; Rhamnolipid; Sophorolipid

Indexed keywords

HYDROCARBON; PETROLEUM; RHAMNOLIPID;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOREMEDIATION; CARBON SOURCE; CONTROLLED STUDY; ENRICHMENT CULTURE; GEL CHROMATOGRAPHY; INFRARED SPECTROSCOPY; LIQUID LIQUID EXTRACTION; MASS SPECTROMETRY; MATHEMATICAL PARAMETERS; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MICROBIAL CONSORTIUM; NONHUMAN; PARACOCCUS; PHYLOGENY; STRUCTURE ANALYSIS; THIN LAYER CHROMATOGRAPHY;

ALCANIVORAX; BACTERIA (MICROORGANISMS); PARACOCCUS MARCUSII;

EID: 84930939963     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00274     Document Type: Article

References (60)

1. Al-Tahhan, R. A., Sandrin, T. R., Bodour, A. A., and Maier, R. M. (2000). Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl. Environ. Microbiol. 66, 3262-3268. doi: 10.1128/AEM.66.8.3262-3268.2000.
2. Asmer, H. J., Lang, S., Wagner, F., and Wray, V. (1988). Microbial production, structure elucidation and bioconversion of sophorose lipids. J. Am. Oil Chem. Soc. 65, 1460-1466. doi: 10.1007/BF02898308.
3. Banat, I. M., Franzetti, A., Gandolfi, I., Bestetti, G., Martinotti, M. G., Fracchia, L., et al. (2010). Microbial biosurfactants production, applications and future potential. Appl. Microbiol. Biotechnol. 87, 427-444. doi: 10.1007/s00253-010-2589-0.
4. Banat, I. M., Makkar, R. S., and Cameotra, S. S. (2000). Potential commercial applications of microbial surfactants. Appl. Microbiol. Biotechnol. 53, 495-508. doi: 10.1007/s002530051648.
5. Banat, I. M., Satpute, S. K., Cameotra, S. S., Patil, R., and Nyayanit, N. V. (2014). Cost effective technologies and renewable substrates for biosurfactants' production. Front. Microbiol. 5:697. doi: 10.3389/fmicb.2014.00697.
6. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336. doi: 10.1038/nmeth.f.303.
7. Chaerun, S. K., Tazaki, K., Asada, R., and Kogure, K. (2004). Bioremediation of coastal areas 5 years after the Nakhodka oil spill in the Sea of Japan: isolation and characterization of hydrocarbon-degrading bacteria. Environ. Int. 30, 911-922. doi: 10.1016/j.envint.2004.02.007.
8. Cui, Z., Lai, Q., Dong, C., and Shao, Z. (2008). Biodiversity of polycyclic aromatic hydrocarbon-degrading bacteria from deep sea sediments of the Middle Atlantic Ridge. Environ. Microbiol. 10, 2138-2149. doi: 10.1111/j.1462-2920.2008.01637.x.
9. Daniel, H.-J., Reuss, M., and Syldatk, C. (1998). Production of sophorolipids in high concentration from deproteinized whey and rapeseed oil in a two stage fed batch process using Candida bombicola ATCC 22214 and Cryptococcus curvatus ATCC 20509. Biotechnol. Lett. 20, 1153-1156. doi: 10.1023/A:1005332605003.
10. Darvishi, P., Ayatollahi, S., Mowla, D., and Niazi, A. (2011). Biosurfactant production under extreme environmental conditions by an efficient microbial consortium, ERCPPI-2. Colloids Surf. B Biointerfaces 84, 292-300. doi: 10.1016/j.colsurfb.2011.01.011.
11. Diez, S., Jover, E., Bayona, J. M., and Albaiges, J. (2007). Prestige oil spill. III. fate of a heavy oil in the marine environment. Environ. Sci. Technol. 41, 3075-3082. doi: 10.1021/es0629559.
12. Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461. doi: 10.1093/bioinformatics/btq461.
13. Fodelianakis, S., Papageorgiou, N., Karakassis, I., and Ladoukakis, E. D. (2014). Community structure changes in sediment bacterial communities along an organic enrichment gradient associated with fish farming. Ann. Microbiol. 65, 331-335. doi: 10.1007/s13213-014-0865-4.
14. Fredrickson, J. K., Romine, M. F., Beliaev, A. S., Auchtung, J. M., Driscoll, M. E., Gardner, T. S., et al. (2008). Towards environmental systems biology of Shewanella. Nat. Rev. Microbiol. 6, 592-603. doi: 10.1038/nrmicro1947.
15. García-Rivero, M., Saucedo-Castañeda, G., and Gutiérrez-Rojas, M. (2007). Organic solvents improve hydrocarbon desorption and biodegradation in highly contaminated weathered soils. J. Environ. Eng. Sci. 6, 389-395. doi: 10.1139/s06-061.
16. Golyshin, P. N., Martins Dos Santos, V. A. P., Kaiser, O., Ferrer, M., Sabirova, Y. S., and Lünsdorf, H. (2003). Genome sequence completed of Alcanivorax borkumensis, a hydrocarbon-degrading bacterium that plays a global role in oil removal from marine systems. J. Biotechnol. 106, 215-220. doi: 10.1016/j.jbiotec.2003.07.013.
17. Good, I. J. (1953). The population frequencies of species and the estimation of population parameters. Biometrika 40, 237-264. doi: 10.1093/biomet/40.3-4.237.
18. Harker, M., Hirschberg, J., and Oren, A. (1998). Paracoccus marcusii sp. nov., an orange Gram-negative coccus. International. J. Syst. Bacteriol. 48, 543-548. doi: 10.1099/00207713-48-2-543.
19. Hassanshahian, M., Emtiazi, G., and Cappello, S. (2012). Isolation and characterization of crude-oil-degrading bacteria from the Persian Gulf and the Caspian Sea. Mar. Pollut. Bull. 64, 7-12. doi: 10.1016/j.marpolbul.2011.11.006.
20. Helvaci, S., Peker, S., and Ozdemir, G. (2004). Effect of electrolytes on the surface behavior of rhamnolipids R1 and R2. Colloids Surf. B Biointerfaces 35, 225-233. doi: 10.1016/j.colsurfb.2004.01.001.
21. Hirschberg, J., and Harker, M. (1999). Carotenoid-producing bacterial species and process for production of carotenoids using same (Google Patents). US Patent 5935808.
22. Ibacache-Quiroga, C., Ojeda, J., Espinoza-Vergara, G., Olivero, P., Cuellar, M., and Dinamarca, M. A. (2013). The hydrocarbon-degrading marine bacterium Cobetia sp. strain MM1IDA2H-1 produces a biosurfactant that interferes with quorum sensing of fish pathogens by signal hijacking. Microb. Biotechnol. 6, 394-405. doi: 10.1111/1751-7915.12016.
23. ITOPF. (2013). International Tanker Owners Pollution Federation. Available at: http://www.itopf.com/information-services/data-and-statistics/statistics/.
24. Jiménez, N., Viñas, M., Guiu-Aragonés, C., Bayona, J., Albaigés, J., and Solanas, A. (2011). Polyphasic approach for assessing changes in an autochthonous marine bacterial community in the presence of Prestige fuel oil and its biodegradation potential. Appl. Microbiol. Biotechnol. 91, 823-834. doi: 10.1007/s00253-011-3321-4.
25. Kostka, J. E., Prakash, O., Overholt, W. A., Green, S. J., Freyer, G., Canion, A., et al. (2011). Hydrocarbon-degrading bacteria and the bacterial community response in gulf of Mexico beach sands impacted by the deepwater horizon oil spill. Appl. Environ. Microbiol. 77, 7962-7974. doi: 10.1128/AEM.05402-11.
26. Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D., et al. (2012). Experimental and analytical tools for studying the human microbiome. Nat. Rev. Genet. 13, 47-58. doi: 10.1038/nrg3129.
27. Marchant, R., and Banat, I. M. (2012). Microbial biosurfactants: challenges and opportunities for future exploitation. Trends Biotechnol. 30, 558-565. doi: 10.1016/j.tibtech.2012.07.003.
28. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., et al. (2012). An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618. doi: 10.1038/ismej.2011.139.
29. McGenity, T. J., Folwell, B. D., McKew, B. A., and Sanni, G. O. (2012). Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat. Biosyst. 8, 10. doi: 10.1186/2046-9063-8-10.
30. Mnif, S., Chamkha, M., and Sayadi, S. (2009). Isolation and characterization of Halomonas sp. strain C2SS100, a hydrocarbon-degrading bacterium under hypersaline conditions. J. Appl. Microbiol. 107, 785-794. doi: 10.1111/j.1365-2672.2009.04251.x.
31. Moore, E., Arnscheidt, A., Kruger, A., Strompl, C., and Mau, M. (2004). "Simplified protocols for the preparation of genomic DNA from bacterial cultures," in Molecular Microbial Ecology Manual, 2 Edn, eds G. Kowalchuk, F. de Bruijn, I. M. Head, A. J. Van der Zijpp, and J. D. van Elsas (Dordrecht: Kluwer Academic Publishers), 3-18.
32. Mukherjee, S., Das, P., Sivapathasekaran, C., and Sen, R. (2008). Enhanced production of biosurfactant by a marine bacterium on statistical screening of nutritional parameters. Biochem. Eng. J. 42, 254-260. doi: 10.1016/j.bej.2008.07.003.
33. National Research Council (NRC) of the National Academies-Committee on Oil in the Sea. (2003). Oil in the Sea III:Inputs, Fates, and Effects. Washington: The National Academies Press.
34. Nguyen, T. T., and Sabatini, D. A. (2011). Characterization and emulsification properties of rhamnolipid and sophorolipid biosurfactants and their applications. Int. J. Mol. Sci. 12, 1232-1244. doi: 10.3390/ijms12021232.
35. Nguyen, T. T., Youssef, N. H., McInerney, M. J., and Sabatini, D. A. (2008). Rhamnolipid biosurfactant mixtures for environmental remediation. Water Res. 42, 1735-1743. doi: 10.1016/j.watres.2007.10.038.
36. Nikolopoulou, M., and Kalogerakis, N. (2008). Enhanced bioremediation of crude oil utilizing lipophilic fertilizers combined with biosurfactants and molasses. Mar. Pollut. Bull. 56, 1855-1861. doi: 10.1016/j.marpolbul.2008.07.021.
37. Nikolopoulou, M., and Kalogerakis, N. (2010). "Biostimulation strategies for enhanced bioremediation of marine oil spills including chronic pollution," in Handbook of Hydrocarbon and Lipid Microbiology, ed. K. Timmis (Berlin: Springer), 2521-2529.
38. Nikolopoulou, M., Pasadakis, N., and Kalogerakis, N. (2013a). Evaluation of autochthonous bioaugmentation and biostimulation during microcosm-simulated oil spills. Mar. Pollut. Bull. 72, 165-173. doi: 10.1016/j.marpolbul.2013.04.007.
39. Nikolopoulou, M., Pasadakis, N., Norf, H., and Kalogerakis, N. (2013b). Enhanced ex situ bioremediation of crude oil contaminated beach sand by supplementation with nutrients and rhamnolipids. Mar. Pollut. Bull. 77, 37-44. doi: 10.1016/j.marpolbul.2013.10.038.
40. Nuñez, A., Ashby, R., Foglia, T. A., and Solaiman, D. K. Y. (2001). Analysis and characterization of sophorolipids by liquid chromatography with atmospheric pressure chemical ionization. Chromatographia 53, 673-677. doi: 10.1007/BF02493019.
41. Pouli, M., Fava, F., and Agathos, S. N. (2008). "Role of a (Paracoccus) strain in the degradation and bioremediation of polycyclic aromatic hydrocarbons," in Proceedings of the Bio Remediation, Bologna.
42. Quince, C., Lanzen, A., Davenport, R., and Turnbaugh, P. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12:38. doi: 10.1186/1471-2105-12-38.
43. Raaijmakers, J. M., de Bruijn, I., Nybroe, O., and Ongena, M. (2010). Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol. Rev. 34, 1037-1062. doi: 10.1111/j.1574-6976.2010.00221.x.
44. Rahman, K. S. M., Rahman, T. J., Lakshmanaperumalsamy, P., Marchant, R., and Banat, I. M. (2003). The potential of bacterial isolates for emulsification with a range of hydrocarbons. Acta Biotechnol. 23, 335-345. doi: 10.1002/abio.200390043.
45. Rahman, P. K. S. M., and Gakpe, E. (2008). Production, characterisation and applications of biosurfactants-Review. Biotechnology 7, 360-370. doi: 10.3923/biotech.2008.360.370.
46. Randhawa, K. K. S., and Rahman, P. K. S. M. (2014). Rhamnolipid biosurfactants-past, present, and future scenario of global market. Front. Microbiol. 5:454. doi: 10.3389/fmicb.2014.00454.
47. Schneiker, S., Dos Santos, V. A. P. M., Bartels, D., Bekel, T., Brecht, M., and Buhrmester, J. (2006). Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat. Biotechnol. 24, 997-1004. doi: 10.1038/nbt1232.
48. Silverstein, R. M., and Webster, F. X. (1998). Spectrometric Identification of Organic Compounds. New York, NY: Wiley.
49. Smyth, T. J. P., Perfumo, A., Marchant, R., and Banat, I. M. (2010). "Isolation and analysis of low molecular weight microbial glycolipids," in Handbook of Hydrocarbon and Lipid Microbiology, ed. K. N. Timmis (Berlin: Springer-Verlag), 3705-3723. doi: 10.1007/978-3-540-77587-4_291.
50. Sotirova, A., Spasova, D., Vasileva-Tonkova, E., and Galabova, D. (2009). Effects of rhamnolipid-biosurfactant on cell surface of Pseudomonas aeruginosa. Microbiol. Res. 164, 297-303. doi: 10.1016/j.micres.2007.01.005.
51. Thomas, J. C., Wafula, D., Chauhan, A., Green, S. J., Gragg, R., and Jagoe, C. (2014). A survey of deepwater horizon (DWH) oil-degrading bacteria from the eastern oyster biome and its surrounding environment. Front. Microbiol. 5:12. doi: 10.3389/fmicb.2014.00149.
52. Top, E. M., and Springael, D. (2003). The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr. Opin. Biotechnol 14, 262-269. doi: 10.1016/S0958-1669(03)00066-1.
53. Trejo-Castillo, R., Martínez-Trujillo, M. A., and García-Rivero, M. (2014). Effectiveness of crude biosurfactant mixture for enhanced biodegradation of hydrocarbon contaminated soil in slurry reactor. Int. J. Environ. Res. 8, 727-732.
54. Ventikos, N. P., and Sotiropoulos, F. S. (2014). Disutility analysis of oil spills: graphs and trends. Mar. Pollut. Bull. 81, 116-123. doi: 10.1016/j.marpolbul.2014.02.007.
55. Wei, Y.-H., Chou, C.-L., and Chang, J.-S. (2005). Rhamnolipid production by indigenous Pseudomonas aeruginosa J4 originating from petrochemical wastewater. Biochem. Eng. J. 27, 146-154. doi: 10.1016/j.bej.2005.08.028.
56. Weisburg, W. G., Barns, S. M., Pelletier, D. A., and Lane, D. J. (1991). 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173, 697-703.
57. Whang, M., Liu, P. W., Ma, C. C., and Cheng, S. S. (2008). Application of biosurfactants, rhamnolipid, and surfactin, for enhanced biodegradation of diesel-contaminated water and soil. J. Hazard. Mater. 151, 155-163. doi: 10.1016/j.jhazmat.2007.05.063.
58. Yakimov, M. M., Golyshin, P. N., Lang, S., E.Moore, R. B., Abraham, W. R., Lünsdorf, H., et al. (1998). Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int. J. Syst. Bacteriol. 48, 339-348. doi: 10.1099/00207713-48-2-339.
59. Yakimov, M. M., Timmis, K. N., and Golyshin, P. N. (2007). Obligate oil-degrading marine bacteria. Curr. Opin. Biotechnol. 18, 257-266. doi: 10.1016/j.copbio.2007.04.006.
60. Youssef, N. H., Duncan, K. E., Nagle, D. P., Savage, K. N., Knapp, R. M., and McInerney, M. J. (2004). Comparison of methods to detect biosurfactant production by diverse microorganisms. J. Microbiol. Methods 56, 339-347. doi: 10.1016/j.mimet.2003.11.001.