Abstract
The replacement of synthetic surface-active compounds (SACs) by their microbial counterparts is carving out a niche for themselves in the field of bioremediation. However, the high cost of microbial products has limited their application at a realistic scale. In the current study, several hydrocarbon-degrading microorganisms were assayed as potential SAC producers in low-cost liquid media. Only the strain CC10, placed within the class Actinobacteria, was able to produce emulsifying molecules by using a combination of sugarcane vinasse or crude glycerol (as cheap carbon substrates) with urea or peptone (as nitrogen sources). The emulsifying activity of the supernatants and the stability of emulsions formed with motor oil depended on the carbon and nitrogen sources. However, the biodegradability of these metabolites was only associated with the carbon substrate, and it was always higher than the two tested synthetic surfactants, sodium dodecyl sulfate and Triton X-100. Also, a positive linear association between emulsifying and lipase activities of the CC10 supernatants was detected (r = 0.781; p = 0.219), with the maximum activities detected in the glycerol-peptone supernatant. Interestingly, this supernatant was able to emulsify different oily substrates, a property that could be used to increase the efficiency of the treatment of effluents with high fat content.
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A.P.H.A., A.W.W.A., & W.E.F. (2012). Standard methods for examination of water and wastewater (22nd ed.). Washington: American public health association 1360 pp. ISBN 978–087553–013-0.
Albarracín, V. H., Amoroso, M. J., & Abate, C. M. (2005). Isolation and characterization of indigenous copper-resistant actinomycete strains. Chemie der Erde-Geochemistry, 65, 145–156.
Ayed, H. B., Jemil, N., Maalej, H., Bayoudh, A., Hmidet, N., & Nasri, M. (2015). Enhancement of solubilization and biodegradation of diesel oil by biosurfactant from Bacillus amyloliquefaciens. International Biodeterioration and Biodegradation, 99, 8–14.
Bosch, M. P., Robert, M., Mercade, M. E., Espuny, M. J., Parra, J. L., & Guinea, J. (1988). Surface-active compounds on microbial cultures. Tenside Surfactants Detergents, 25, 208–211.
Bourguignon, N. (2016). Estudio fisiológico y molecular de la degradación aeróbica de hidrocarburos aromáticos policíclicos (HAPs) por actinomycetes autóctonos, PhD thesis, Universidad Nacional de Tucumán, Argentina.
Cammarota, M. C., & Freire, D. M. G. (2006). A review on hydrolytic enzymes in the treatment of wastewaters with high oil and grease content. Bioresource Technology, 97, 2195–2210.
Carrillo, P., Mardaraz, C., Pitta-Alvarez, S., & Giulietti, A. M. (1996). Isolation and selection of biosurfactant-producing bacteria. World Journal Microbiology and Biotechnology, 12, 82–84.
Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y., Brown, C. T., Porras-Alfaro, A., Kuske, C. R., & Tiedje, J. M. (2014). Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42, 633–642.
Colin, V. L., Castro, M. F., Amoroso, M. J., & Villegas, L. B. (2013a). Production of bioemulsifiers by Amycolatopsis tucumanensis DSM 45259 and their potential application in remediation technologies for soils contaminated with hexavalent chromium. Journal of Hazardous and Materials, 26, 577–583.
Colin, V. L., Pereira, C. E., Villegas, L. B., Amoroso, M. J., & Abate, C. M. (2013b). Production and partial characterization of bioemulsifier from a chromium-resistant actinobacteria. Chemosphere, 90, 1372–1378.
Colin, V. L., Juárez Cortes, A. A., Rodríguez, A., & Amoroso, M. J. (2014). Surface-active compounds of microbial origin and their potential application in technologies of environmental remediation. In A. Alvarez & M. A. Polti (Eds.), Bioremediation in Latin America: current research and perspectives (pp. 255–264). New York: Springer.
Colin, V. L., Juárez Cortes, A. A., Aparicio, J. D., & Amoroso, M. J. (2016). Potential application of a bioemulsifier-producing actinobacterium for treatment of vinasse. Chemosphere, 144, 842–847.
Colla, L. M., Rizzardi, J., Heidtmann Pinto, M., Oliveira Reinehr, C., Bertolin, T. E., & Costa, J. A. (2010). Simultaneous production of lipases and biosurfactants by submerged and solid-state bioprocesses. Bioresource Technology, 101, 8308–8314.
Cooper, D. G., & Goldenberg, B. G. (1987). Surface-active agents from two Bacillus species. Applied and Environmental Microbiology, 53, 224–229.
Damasceno, F. R. C., Cammarota, M. C., & Freire, D. M. G. (2012). The combined use of a biosurfactant and an enzyme preparation to treat an effluent with a high fat content. Colloids and Surfaces B, 95, 241–246.
Doshi, D. V., Maniyar, J. P., Bhuyan, S. S., & Mujumdar, S. S. (2010). Studies on bioemulsifiers production by Actinopolyspora sp. A18 isolated from garden soil. Indian Journal of Biotechnology, 9, 391–396.
Ellis, R. J., Thompson, I. P., & Bailey, M. J. (1999). Temporal fluctuations in the pseudomonal population associated with sugar beet leaves. FEMS Microbiology Ecology, 28, 345–356.
Eraqi, W.A., Yassin, A.S., Ali, A.E., & Amin, M.A. (2016). Utilization of crude glycerol as a substrate for the production of rhamnolipid by Pseudomonas aeruginosa. Biotechnology Research International, 2016(2016), 9.
European Parliament Regulation (EC) (2004). No 648/2004 of the European Parliament and of the Council of 31 March 2004 on detergents. (OJ L 104, 8.4.2004, pp. 1–35).
Franzetti, A., Gandolfi, I., Bertolini, V., Raimondi, C., Piscitello, M., Papacchini, M., & Bestetti, G. (2011). Phylogenetic characterization of bioemulsifier-producing bacteria. International Biodeterioration and Biodegradation, 65, 1095–1099.
Fuentes, M. S., Benimeli, C. S., Cuozzo, S. A., & Amoroso, M. J. (2010). Isolation of pesticide degrading actinomycetes from a contaminated site: bacterial growth, removal and dechlorination of organochlorine pesticides. International Biodeterioration and Biodegradation, 64, 434–441.
George, S., & Jayachandran, K. (2013). Production and characterization of rhamnolipid biosurfactant from waste frying coconut oil using a novel Pseudomonas aeruginosa D. Journal of Applied Microbiology, 114(2), 373–383.
Gheorghe, S., Lucaciu, I., Paun, I., Stoica, C., & Stanescu, E. (2013). Ecotoxicological behavior of some cationic and amphoteric surfactants (biodegradation, toxicity and risk assessment). In R. Chamy & F. Rosenkranz (Eds.), Biodegradation-Life of Science (pp. 83–114). Rijeka: InTech.
Gudiña, E. J., Pereira, J. F. B., Costa, R., Evtuguin, D. V., Coutinho, J. A. P., Teixeira, J. A., & Rodrigues, L. R. (2015). Novel bioemulsifier produced by a Paenibacillus strain isolated from crude oil. Microbial Cell Factories, 14, 14.
Guerra de Oliveira, J., & Garcia-Cruz, C. H. (2013). Properties of a biosurfactant produced by Bacillus pumilus using vinasse and waste frying oil as alternative carbon sources. Brazilian Archives of Biology and Technology, 56, 155–160.
Gutnick, D., Bach, H., & Berdichevsky, Y. (2003). An exocellular protein from the oildegrading microbe Acinetobacter venetianus RAG-1 enhances the emulsifying activity of the polymeric bioemulsifier emulsan. Applied and Environmental Microbiology, 69, 2608–2615.
Hanna, S., Sekhon, K. K., & Prakash, N. T. (2009). Cloning and expression of a biosurfactant gene from endosulfan degrading Bacillus sp: correlation between esterase activity and biosurfactant production. Biotechnology, 8, 235–241.
Hayder, N. H., Alaa, S., & Abdulamalik, H. (2014). Optimized conditions for bioemulsifier production by local Streptomyces sp. SS 20 isolated from hydrocarbon contaminated soil. Romanian Biotechnological Letters, 19(1), 8979–8993.
Jukes, T. H., & Cantor, C. R. (1969). Evolution of protein molecules. Mammalian Protein Metabolism, 3, 121–132.
Khopade, A., Ren, B., Liu, X.-Y., Mahadik, K., Zhang, L., & Kokare, C. (2012). Production and characterization of biosurfactant from marine Streptomyces species B3. Journal of Colloid and Interface Science, 367, 311–318.
Kim, K. O., Shin, K. S., Kim, M. N., Shin, K. S., Labeda, D. P., Han, J. H., & Kim, S. B. (2012). Reassessment of the status of Streptomyces setonii and reclassification of Streptomyces fimicarius as a later synonym of Streptomyces setonii and Streptomyces albovinaceus as a later synonym of Streptomyces globisporus based on combined 16s rRNA/gyrB gene. International Journal of Systematic and Evolutionary Microbiology, 62, 2978–2985.
Kiran, G. S., Sabarathnam, B., Thajuddin, N., & Selvin, J. (2014). Production of glycolipid biosurfactant from Sponge-associated marine actinobacterium Brachybacterium paraconglomeratum MSA21. Journal of Surfactants and Detergents, 17(3), 531–542.
de Lima, A. M., & Rodríguez de Souza, R. (2014). Use of sugar cane vinasse as substrate for biosurfactant production using Bacillus subtilis PC. Chemical Engineering Transactions, 37, 673–678.
Meliani, A., & Bensoltane, A. (2014). Enhancement of hydrocarbons degradation by use of Pseudomonas biosurfactants and biofilms. Journal of Petroleum and Environmental Biotechnology, 5, 1.
Montero-Rodríguez, D., Andrade, R. F. S., Ramos Ribeiro, D. L., Rubio-Ribeaux, D., Lima, R. A., Araújo, H. W. C., & Campos-Takaki, G. M. (2015). Bioremediation of petroleum derivative using biosurfactant produced by Serratia marcescens UCP/WFCC 1549 in low-cost medium. International Journal of Current Microbiology and Applied Sciences, 4, 550–562.
Motevasel, M. (2014). A study of surface biosurfactants applications on oil degradation. American Journal of Oil and Chemical technologies, 2, 289–294.
Pleissner, D., Qi, Q., Gao, C., Perez Rivero, C., Webb, C., Ki Lin, C. S., & Venus, J. (2016). Valorization of organic residues for the production of added value chemicals: a contribution to the bio-based economy. Biochemical Engineering Journal, 116, 3–16.
Quillaguamán, J., Hatti-Kaul, R., Mattiasson, B., Alvarez, M. T., & Delgado, O. (2004). Halomonas boliviensis sp. nov., an alkalitolerant, moderate halophile isolated from soil around a Bolivian hypersaline lake. International Journal of Systematic Evolutionary Microbiology, 54, 721–725.
Ruggeri, C., Franzetti, A., Bestetti, G., Caredda, P., La Colla, P., Pintus, M., Sergi, S., & Tamburini, E. (2009). Isolation and characterisation of surface active compound-producing bacteria from hydrocarbon-contaminated environments. International Biodeterioration and Biodegradation, 63, 936–942.
Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
Samul, D., Leja, K., & Grajek, W. (2014). Impurities of crude glycerol and their effects on metabolite production. Annals of Microbiology, 64, 891–898.
Sekhon, K. K., Khanna, S., & Cameotra, S. S. (2011). Enhanced biosurfactant production through cloning of three genes and role of esterase in biosurfactant release. Microbial Cells Factories, 10, 49.
Sekhon, K. K., Khanna, S., & Cameotra, S. S. (2012). Biosurfactant production and potential correlation with esterase activity. Journal of Petroleum and Environmental Biotechnology, 3, 7.
Silva, J. N., Estrada Gutarra, M. L., Freire, D. M. G., & Cammarota, M. C. (2013). Application of home-made enzyme and biosurfactant in the anaerobic treatment of effluent with high fat content. Journal Bioprocessing and Biotechniques, 3, 139.
de Souza Monteiro, A., Souza Domingues, V., Souza, M. V. D., Lula, I., Bonoto Gonçalves, D., Pessoa de Siqueira, E., & dos Santos, V. L. (2012). Bioconversion of biodiesel refinery waste in the bioemulsifier by Tricchosporon mycotoxinivorans CLA2. Biotechnology for Biofuels, 5, 29.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsinomy methods. Molecular Biology and Evolution, 28, 2731–2739.
Tcholakova, S., Denkov, N., Ivanov, I. B., & Marinov, R. (2004). Evaluation of short-term and long-term stability of emulsions by centrifugation and NMR. Bulgarian Journal of Physics, 31, 96–110.
Usman, M. M., Dadrasnia, A., Lim, K. T., Mahmud, A. F., & Ismail, S. (2016). Applicationof biosurfactants in environmental biotechnology; remediation of oil and heavy metal. AIMS Bioengineering, 3, 289–304.
Uzoigwe, C., Burgess, J. G., Ennis, C. J., & Rahman, P. K. S. M. (2015). Bioemulsifiers are not biosurfactants and require different screening approaches. Frontiers in Microbiology, 6, 245.
Valerio, O., Horvath, T., Pond, C., Misra, M., & Mohanty, A. (2015). Improved utilization of crude glycerol from biodiesel industries: synthesis and characterization of sustainable biobased polyesters. Industrial Crops and Products, 78, 141–147.
Winkler, U. K., & Stuckman, M. (1979). Glycogen, hyaluronate, and some other polysaccharides greatly enhance the formation of exo-lipase by Serratia marescens. Journal of Bacteriology, 138, 663–670.
Acknowledgements
This work was supported by the National Agency for the Promotion of Science and Technology, Argentina (PICT 2012-2920) and the National Research Council of Argentina, CONICET, Argentina (PIP 470-13). The authors gratefully acknowledge the technical assistance of Mr. Guillermo Borchia. We also thank Mr. Eric Fengler for his review of the English style.
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Colin, V.L., Bourguignon, N., Gómez, J.S. et al. Production of Surface-Active Compounds by a Hydrocarbon-Degrading Actinobacterium: Presumptive Relationship with Lipase Activity. Water Air Soil Pollut 228, 454 (2017). https://doi.org/10.1007/s11270-017-3623-y
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DOI: https://doi.org/10.1007/s11270-017-3623-y