Simultaneous Production of Lipases and Biosurfactants in Solid-State Fermentation and Use in Bioremediation
Publication: Journal of Environmental Engineering
Volume 146, Issue 9
Abstract
This study investigated the simultaneous production of lipases and biosurfactants and the use of culture media containing biocompounds (without precipitation and purification processes) in the bioremediation of contaminated soil. Different concentrations of agroindustrial raw materials, moisture, oil inducers, and nitrogen were studied. The bioremediation assay was evaluated for 90 days, using biodiesel as a contaminant, adding fermented solid culture medium in soil and comparing it to natural attenuation. The culture media was composed of wheat bran:corncob (proportion ), 5% inducer, and 60% moisture, inoculated with Aspergillus niger, allowing the simultaneous production of biosurfactants [ Units of Emulsifying activity (UE)] and lipases [ Units of Lipase (U)]. In the bioremediation assay, the highest degradation of contaminant (64.09%) was found after 60 days using 10% of the fermented solid culture medium containing lipases and biosurfactants. Coproduction of both biocompounds in the fermentation process was allowed, leading to cost reductions and the viability potential of the bioprocess on an industrial production scale, as well as its environmental application in the treatment of oily contaminants.
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Data Availability Statement
All data, models, and code generated or used during the study appear in the published article.
Acknowledgments
The authors thank the National Council for Scientific and Technological Development (CNPq) for the financial support, Project 408866/2016-0, BS Bios Company for supplying the biodiesel used in this work, and University of Passo Fundo.
References
AOAC (Association of Official Analytical Chemists). 2000. Official methods of analysis of the Association of Official Analytical Chemists International. Washington, DC: AOAC.
Banat, I. M., S. K. Satpute, S. S. Cameotra, R. Patil, and N. N. Nyayanit. 2014. “Cost effective technologies and renewable substrates for biosurfactants’ production.” Front. Microbiol. 5 (Dec): 697. https://doi.org/10.3389/fmicb.2014.00697.
Burkert, J. F. M., F. Maugeri, and M. I. Rodrigues. 2004. “Optimization of extracellular lipase production by Geotrichum sp. using factorial design.” Bioresour. Technol. 91 (1): 77–84. https://doi.org/10.1016/S0960-8524(03)00152-4.
Cavka, A., B. Alriksson, S. H. Rose, W. H. Van Zyl, and L. J. Jönsson. 2014. “Production of cellulosic ethanol and enzyme from waste fiber sludge using SSF, recycling of hydrolytic enzymes and yeast, and recombinant cellulase-producing Aspergillus niger.” J. Ind. Microbiol. Biotechnol. 41 (8): 1191–1200. https://doi.org/10.1007/s10295-014-1457-9.
Cecchin, I., C. Reginatto, A. Thomé, L. M. Colla, and K. R. Reddy. 2016. “Influence of physicochemical factors on biodiesel retention in clayey residual soil.” J. Environ. Eng. 142 (4): 04015093. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001060.
Chu, W., and K. H. Chan. 2003. “The mechanism of the surfactant-aided soil washing system for hydrophobic and partial hydrophobic organics.” Sci. Total Environ. 307 (1): 83–92. https://doi.org/10.1016/S0048-9697(02)00461-8.
Colla, L. M., A. L. Primaz, S. Benedetti, R. A. Loss, M. Lima, C. O. Reineh, T. E. Bertolin, and J. A. V. Costa. 2016. “Surface response methodology for the optimization of lipase production under submerged fermentation by filamentous fungi.” Braz. J. Microbiol. 47 (2): 461–467. https://doi.org/10.1016/j.bjm.2016.01.028.
Colla, L. M., J. Rizzardi, M. H. Pinto, C. O. Reinehr, T. E. Bertolin, and J. A. V. Costa. 2010. “Simultaneous production of lipases and biosurfactants by submerged and solid-state bioprocesses.” Bioresour. Technol. 101 (21): 8308–8314. https://doi.org/10.1016/j.biortech.2010.05.086.
Contesini, F. J., D. B. Lopes, G. A. Macedo, M. G. Nascimento, and P. O. Carvalho. 2010. “Aspergillus sp. lipase: Potential biocatalyst for industrial use.” J. Mol. Catal. B: Enzym. 67 (3–4): 163–171. https://doi.org/10.1016/j.molcatb.2010.07.021.
Cooper, D. G., and B. G. Goldenberg. 1987. “Surface-active agents from two Bacillus species.” Appl. Environ. Microbiol. 53 (2): 224–229. https://doi.org/10.1128/AEM.53.2.224-229.1987.
Costa, M. J., L. Moraes, F. Bion, M. Rivera, L. Moura, and M. Conceição. 2000. “Avaliação da eficácia da suplementação com melaço na dieta de ratos normais e depletados.” Arch. Latinoam. Nutr. 50 (4): 341–345.
Costa, T. M., K. L. Hermann, G. Gracia-Roman, R. C. S. C. Valle, and B. B. Tavares. 2017. “Lipase production by Aspergillus niger grown in different agro-industrial wastes by solid-state fermentation.” Braz. J. Chem. Eng. 34 (2): 419–427. https://doi.org/10.1590/0104-6632.20170342s20150477.
Santos, D. K. F., H. M. Meira, R. D. Rufino, and J. M. Luna, and L. A. Sarubbo. 2017. “Biosurfactant production from Candida lipolytica in bioreactor and evaluation of its toxicity for application as a bioremediation agent.” Process. Biochem. 54 (1): 20–27. https://doi.org/10.1016/j.procbio.2016.12.020.
Decesaro, A., A. Rempel, T. S. Machado, A. Thomé, K. Reddy, A. C. Margarites, and L. M. Colla. 2016. “Bioremediation of soil contaminated with diesel and biodiesel fuel using biostimulation with microalgae biomass.” J. Environ. Eng. 143 (4): 04016091. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001165.
Flueri, L. F., M. C. Oliveira, M. L. C. Arcuri, B. L. Capoville, M. S. Pereira, C. H. O. Delgado, and P. K. Novelli. 2014. “Production of fungal lipases using wheat bran and soybean bran and incorporation of sugarcane bagasse as a co-substrate in solid-state fermentation.” Food Sci. Biotechnol. 23 (4): 1199–1205. https://doi.org/10.1007/s10068-014-0164-7.
Fontes, G. C., P. F. F. Amaral, and M. A. Z. Coelho. 2008. “Produção de biossurfactante por levedura.” Química Nova 31 (8): 2091–2099. https://doi.org/10.1590/S0100-40422008000800033.
Guerrero, A. B., and E. Muñoz. 2018. “Life cycle assessment of second generation ethanol derived from banana agricultural waste: Environmental impacts and energy balance.” J. Cleaner Prod. 174 (Feb): 710–717. https://doi.org/10.1016/j.jclepro.2017.10.298.
Karigar, C. S., and S. S. Rao. 2011. “Role of microbial enzymes in the bioremediation of pollutants: A review.” Enzyme Res. 2011 (11): 1–11. https://doi.org/10.4061/2011/805187.
Kreling, N. E., M. Zaparoli, A. C. Margarites, M. T. Friedrich, A. Thomé, and L. M. Colla. 2019. “Extracellular biosurfactants from yeast and soil–biodiesel interactions during bioremediation.” Int. J. Environ. Sci. Technol. 17 (1): 395–408. https://doi.org/10.1007/s13762-019-02462-9.
Larik, I. A., M. A. Qazi, A. H. Phulpotp, A. Haleem, S. Ahmed, and N. A. Kanhar. 2019. “Stenotrophomonas maltophilia strain : An efficient biosurfactant-producing bacterium for biodegradation of diesel oil and used engine oil.” Int. J. Environ. Sci. Technol. 16 (1): 259–268. https://doi.org/10.1007/s13762-018-1666-2.
Lima, B. M. 2012. “Produção de biossurfactantes pelos fungos Aspergillus ochraceus e Penicillium expansum em fermentação semi-sólida utilizando resíduos agroindustriais como substrato.” Dissertation (Master in Microbiology), Paulista State Univ. Julio de Mesquita Filho, Institute of Biosciences, Letters and Exact Sciences.
Lizardi-Jiménez, M. A., and R. Hernández-Martínez. 2017. “Solid state fermentation (SSF): Diversity of applications to valorize waste and biomass.” 3 Biotech 7 (1): 44. https://doi.org/10.1007/s13205-017-0692-y.
Machado, T. S., A. Decesaro, A. C. Cappellaro, B. S. Machado, K. S. Reginato, C. O. Reinehr, A. Thomé, and L. M. Colla. 2020. “Effects of homemade biosurfactant from Bacillus methylotrophicus on bioremediation efficiency of a clay soil contaminated with diesel oil.” Ecotoxicol. Environ. Saf. 201: 110798. https://doi.org/10.1016/j.ecoenv.2020.110798.
Mahadik, N. D., U. S. Puntambekar, K. B. Bastawde, J. M. Khire, and D. V. Gokhale. 2002. “Production of acidic lipase by Aspergillus niger in solid state fermentation.” Process Biochem. 38 (5): 715–721. https://doi.org/10.1016/S0032-9592(02)00194-2.
Miller, G. L. 1959. “Use of dinitrosalicylic acid reagent for determination of reducing sugar.” Anal. Chem. 31 (3): 426–428. https://doi.org/10.1021/ac60147a030.
Oliveira, F., C. E. Souza, V. R. O. L. Peclat, J. M. Salgado, B. D. Robeiro, M. A. Z. Coelho, A. Venâncio, and I. Belo. 2017. “Optimization of lipase production by Aspergillus ibericus from oil cakes and its application in esterification reactions.” Food Bioprod. Process. 102 (Mar): 268–277. https://doi.org/10.1016/j.fbp.2017.01.007.
Pandey, A. 2003. “Solid-state fermentation.” Biochem. Eng. J. 13 (2–3): 81–84. https://doi.org/10.1016/S1369-703X(02)00121-3.
Perfumo, A., I. M. Banat, and R. Marchant. 2018. “Going green and cold: Biosurfactants from low-temperature environments to biotechnology applications.” Trends Biotechnol. 36 (3): 277–289. https://doi.org/10.1016/j.tibtech.2017.10.016.
Quintella, C. M., A. M. T. Mata, and L. C. P. Lima. 2019. “Overview of bioremediation with technology assessment and emphasis on fungal bioremediation of oil contaminated soils.” J. Environ. Manage. 241 (Jul): 156–166. https://doi.org/10.1016/j.jenvman.2019.04.019.
Raj, T., M. Kapoor, R. Gaur, J. Christopher, B. Y. Lamba, D. K. Tuli, and R. Kumar. 2015. “Physical and chemical characterization of various Indian agriculture residues for biofuels production.” Energy Fuels 29 (5): 3111–3118. https://doi.org/10.1021/ef5027373.
Reinehr, C. O., L. Bortoluzzi, V. Q. Morais, T. M. Smaniotto, C. K. Zen, D. Oliveira, and H. Treichel. 2016. “Produção de lipases com atividade de hidrólise por Aspergillus utilizando subprodutos agroindustriais, óleo de soja e glicerol.” Revista Ciências Exatas e Naturais 18 (1): 97–115. https://doi.org/10.5935/RECEN.2016.01.05.
Riffaldi, R., R. Levi-Minzi, R. Cardelli, S. Palumbo, and A. Saviozzi. 2006. “Soil biological activities in monitoring the bioremediation of diesel oil-contaminated soil.” Water Air Soil Pollut. 170 (1–4): 3–15. https://doi.org/10.1007/s11270-006-6328-1.
Rodrigues, E. F., C. O. Reinehr, T. E. Bertolin, and L. M. Colla. 2014. “Produção de compostos com propriedades emulsificantes por Aspergillus flavus utilizando resíduos agroindustriais.” Revista Ciências Exatas e Naturais 16 (1): 75–93. https://doi.org/10.5935/RECEN.2014.01.05.
Salim, A. A., S. Grbavcie, N. Sekuljica, A. Stefanovic, S. J. Tanaskovic, N. Lukovic, and Z. K. Jugovic. 2017. “Production of enzymes by a newly isolated Bacillus sp. TMF-1 in solid state fermentation on agricultural by-products: The evaluation of substrate pretreatment methods.” Bioresour. Technol. 228 (Mar): 193–200. https://doi.org/10.1016/j.biortech.2016.12.081.
Salgado, J. M., L. Abrunhosa, A. Venâncio, J. M. Domínguez, and I. Belo. 2016. “Combined bioremediation and enzyme production by Aspergillus sp. in olive mill and winery wastewaters.” Int. Biodeterior. Biodegrad. 110 (May): 16–23. https://doi.org/10.1016/j.ibiod.2015.12.011.
Santos, R. R., L. N. M. Muruci, M. C. T. Damaso, J. P. L. Silva, and L. O. Santos. 2014. “Lipase production by Aspergillus niger 11T53A14 in wheat bran using experimental design methodology.” J. Food Nutr. Res. 2 (10): 659–663. https://doi.org/10.12691/jfnr-2-10-1.
Satpute, S. K., A. G. Banpurkar, P. K. Dhakephalkar, I. M. Banat, and B. A. Chopade. 2010. “Methods for investigating biosurfactants and bioemulsifiers: A review.” Crit. Rev. Biotechnol. 30 (2): 127–144. https://doi.org/10.3109/07388550903427280.
Scherhaufer, S., G. Moates, H. Hartikainen, K. Waldron, and G. Obersteiner. 2018. “Environmental impacts of food waste in Europe.” Waste Manage. 77 (Jul): 98–113. https://doi.org/10.1016/j.wasman.2018.04.038.
Sena, H. H., M. A. Sanches, D. F. S. Rocha, W. O. P. F. Segundo, E. S. Souza, and J. V. B. Souza. 2018. “Production of biosurfactants by soil fungi isolated from the Amazon forest.” Int. J. Microbiol. 2018: 1–8. https://doi.org/10.1155/2018/5684261.
Silva, S. N. R. L., C. B. B. Farias, R. D. Rufino, J. M. Luna, and L. A. Sarubbo. 2010. “Glycerol as substrate for the production of biosurfactant by Pseudomonas aeruginosa UCP0992.” Colloids Surf., B 79 (1): 174–183. https://doi.org/10.1016/j.colsurfb.2010.03.050.
Singh, P., Y. Patil, and V. Rale. 2019. “Biosurfactant production: Emerging trends and promising strategies.” J. Appl. Microbiol. 126 (1): 2–13. https://doi.org/10.1111/jam.14057.
Thomé, A., C. Reginatto, I. Checchin, and L. M. Colla. 2014. “Bioventing in a residual clayey soil contaminated with a blend of biodiesel and diesel oil.” J. Environ. Eng. 140 (11): 06014005. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000863.
Tsuji, M., Y. Yokota, K. Shimohara, S. Kudoh, and T. Hoshino. 2013. “An application of wastewater treatment in a cold environment and stable lipase production of Antarctic basidiomycetous yeast Mrakia blollopis.” PLOS One 8 (3): e59376. https://doi.org/10.1371/journal.pone.0059376.
USEPA. 1996. “Method 3550B, ultrasonic extraction.” Accessed July 12, 2014. http://www.trincoll.edu/∼henderso/textfi∼1/416%20notes/3550b.pdf.
Uzoigwe, C., J. G. Burgess, C. J. Ennis, and P. K. S. M. Rahman. 2015. “Bioemulsifiers are not biosurfactants and require different screening approaches.” Front. Microbiol. 6 (Apr): 1–6. https://doi.org/10.3389/fmicb.2015.00245.
Velmurugan, P., H. Hur, V. Balachandar, S. K. Kannan, K. Lee, S. Lee, J. Chae, P. J. Shea, and B. Oh. 2011. “Monascus pigment production by solid-state fermentation with corn cob substrate.” J. Biosci. Bioeng. 112 (6): 590–594. https://doi.org/10.1016/j.jbiosc.2011.08.009.
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Published In
Journal of Environmental Engineering
Volume 146 • Issue 9 • September 2020
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© 2020 American Society of Civil Engineers.
History
Received: Dec 17, 2019
Accepted: Apr 28, 2020
Published online: Jul 8, 2020
Published in print: Sep 1, 2020
Discussion open until: Dec 8, 2020
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