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Production of Surface-Active Compounds by a Hydrocarbon-Degrading Actinobacterium: Presumptive Relationship with Lipase Activity

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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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References

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Cooper, D. G., & Goldenberg, B. G. (1987). Surface-active agents from two Bacillus species. Applied and Environmental Microbiology, 53, 224–229.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Jukes, T. H., & Cantor, C. R. (1969). Evolution of protein molecules. Mammalian Protein Metabolism, 3, 121–132.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Meliani, A., & Bensoltane, A. (2014). Enhancement of hydrocarbons degradation by use of Pseudomonas biosurfactants and biofilms. Journal of Petroleum and Environmental Biotechnology, 5, 1.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Motevasel, M. (2014). A study of surface biosurfactants applications on oil degradation. American Journal of Oil and Chemical technologies, 2, 289–294.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Saitou, N., & Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.

    CAS  Google Scholar 

  • Samul, D., Leja, K., & Grajek, W. (2014). Impurities of crude glycerol and their effects on metabolite production. Annals of Microbiology, 64, 891–898.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

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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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Correspondence to Verónica Leticia Colin.

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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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