Abstract
The aim of this study was to select cultivation conditions for the production of extracellular biosurfactants from Saccharomyces cerevisiae. This yeast has been recognized due to the production of intracellular biosurfactants, and this work presented a technique to produce extracellular biosurfactants, allowing the reduction in costs with downstream processes. We studied the scale up of production in bioreactors and their effects on bioremediation in soils contaminated with biodiesel. Furthermore, we also evaluated the effects of biosurfactant addition on the adsorption of contaminants in these soils. The concentration and types of inducer (glycerol, soybean oil and diesel oil), pH levels and temperatures were studied to maximize the production through factorial designs. The results that obtained the maximum emulsifying production (6.95 UE d−1) were found in the concentration of 5 g L−1 of glycerol, a pH 5.5 and a temperature of 30 °C. In the scale up of the 5 L bioreactor, the maximum productivity of 3.85 UE d−1 was achieved in 2 days. The addition of 0.05%, 0.1% and 0.5% of biosurfactant in soil contaminated with 20% of biodiesel for 90 days allowed a biodegradation of 56.71% with a 0.5% of biosurfactant. For all evaluated conditions, 25% of the biodegradation value should actually be attributed to the adsorption process. The addition of biosurfactants does not affect the retention of the contaminant in the soil, demonstrating that the biosurfactants improved biodegradation without interfering in the adsorption process of the contaminant in the selected soil, which is important in order to avoid influencing the movement processes of contamination plumes.
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Accorsini FR, Mutton MJR, Lemos EGM, Benincasa M (2012) Biosurfactants production by yeasts using soybean oil and glycerol as low cost substrate. Braz J Microbiol 43:116–125. https://doi.org/10.1590/S1517-83822012000100013
Adamczak M, Bednarski W (2000) Influence of medium composition and aeration on the synthesis of biosurfactants produced by Candida antarctica. Biotechnol Lett 22:313–316. https://doi.org/10.1023/A:1005634802997
Alcantara VA, Pajares IG, Simbahan JF, Rubio MDL (2012) Substrate dependent production and isolation of an extracellular biosurfactant from Saccharomyces cerevisiae 2031. Philipp J Sci 141:13–24
Almeida DG, Soares SRDCF, Luna JM, Rufino RD, Santos VA, Sarubbo LA (2017) Response surface methodology for optimizing the production of biosurfactant by Candida tropicalis on industrial waste substrates. Front Microbiol 8:157. https://doi.org/10.3389/fmicb.2017.00157
Alvim GM, Pontes PP (2018) Aeration and sawdust application effects as structural material in the bioremediation of clayey acid soils contaminated with diesel oil. Int Soil Water Conserv Res 6:253–260. https://doi.org/10.1016/j.iswcr.2018.04.002
Aquino PLM (2011) Produção de biossurfactantes a partir de Bacillus velezensis utilizando resíduos agroindustriais como substrato. Dissertation, State University of São Paulo Júlio de Mesquita Filho
Banat IM, Franzetti A, Gandolfi I, Bestetti G, Martinotti MG, Fracchia L, Smyth TJ, Marchant R (2010) Microbial biosurfactants production, applications and future potential. Appl Microbiol Biotechnol 87:427–444. https://doi.org/10.1007/s00253-010-2589-0
Bartha R, Pramer D (1965) Features of a flask and method for measuring the persistence and biological effects of pesticides in soil. Soil Sci 100:68–70
Bednarski W, Adamczak M, Tomasik J, Płaszczyk M (2004) Application of oil refinery waste in the biosynthesis of glycolipids by yeast. Bioresour Technol 95:15–18. https://doi.org/10.1016/j.biortech.2004.01.009
Berg JM, Tymoczko JL, Stryer L (2006) Biochemistry. WH Freeman, New York
Bezza FA, Chirwa EMN (2015) Production and applications of lipopeptide biosurfactant for bioremediation and oil recovery by Bacillus subtilis CN2. Biochem Eng J 101:168–178. https://doi.org/10.1016/j.bej.2015.05.007
Bhardwaj G, Cameotra SS, Chopra HK (2013) Biosurfactants from fungi: a review. J Pet Environ Biotechnol 4:1–6. https://doi.org/10.4172/2157-7463.1000160
Brasil (2014) Law 13033 of September 24, 2014. http://www.planalto.gov.br/ccivil_03/_Ato2011-2014/2014/Lei/L13033.htm. Accessed 5 Nov 2018
Brasil (2016) Law 13263 of March 23, 2016. http://www.planalto.gov.br/ccivil_03/_ato2015-2018/2016/lei/L13263.htm. Accessed 5 Nov 2018
Çakar ZP, Turanlı-Yıldız B, Alkım C, Yılmaz Ü (2012) Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res 12:171–182. https://doi.org/10.1111/j.1567-1364.2011.00775.x
Cecchin I, Reginatto C, Thomé A, Colla LM, Reddy KR (2016) Influence of physicochemical factors on biodiesel retention in clayey residual soil. J Environ Eng 142:1–8. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001060
Chiaranda HS (2011) Alterações biogeoquímicas em águas subterrâneas impactadas por biodiesel de soja e misturas de diesel/biodiesel (B20). Thesis, Federal University of Santa Catarina
Chu W, Chan KH (2003) The mechanism of the surfactant-aided soil washing system for hydrophobic and partial hydrophobic organics. Sci Total Environ 307:83–92. https://doi.org/10.1016/S0048-9697(02)00461-8
Ciapina EM, Melo WC, Santa Anna LM, Santos AS, Freire DM, Pereira N (2006) Biosurfactant production by Rhodococcus erythropolis grown on glycerol as sole carbon source. Appl Biochem Biotechnol 131:880–886. https://doi.org/10.1385/ABAB:131:1:880
Colla TS, Andreazza R, Bücker F, Souza MM, Tramontini L, Prado GR, Frazzon APG, Camargo FAO, Bento FM (2014) Bioremediation assessment of diesel–biodiesel-contaminated soil using an alternative bioaugmentation strategy. Environ Sci Pollut Res 21:2592–2602. https://doi.org/10.1007/s11356-013-2139-2
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229
Costa AG, Magnani M, Castro-Gomez RJH (2012) Obtenção e caracterização de manoproteínas da parede celular de leveduras de descarte em cervejaria. Acta Sci Biol Sci 34:77–84. https://doi.org/10.4025/actascibiolsci.v34i1.7124
Cremonez PA, Feroldi M, Nadaleti WC, Rossi E, Feiden A, Camargo MP, Cremonez FE, Klajn FF (2015) Biodiesel production in Brazil: current scenario and perspectives. Renew Sustain Energy Rev 42:415–428. https://doi.org/10.1016/j.rser.2014.10.004
Decesaro A, Rigon MR, Thomé A, Colla LM (2013) Produção de biossurfactantes por microrganismos isolados de solo contaminado com óleo diesel. Quím Nova 36:947–954
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64
Eldin AM, Kamel Z, Hossam N (2019) Isolation and genetic identification of yeast producing biosurfactants, evaluated by different screening methods. Microchem J 146:309–314. https://doi.org/10.1016/j.microc.2019.01.020
Fai AEC, Simiqueli APR, Andrade CJ, Ghiselli G, Pastore GM (2015) Optimized production of biosurfactant from Pseudozyma tsukubaensis using cassava wastewater and consecutive production of galactooligosaccharides: an integrated process. Biocatal Agric Biotechnol 4:535–542. https://doi.org/10.1016/j.bcab.2015.10.001
Faria AF (2010) Produção, purificação e caracterização química de biossurfactantes produzidos por Bacillus substilis em glicerina residual. Thesis, Campinas State University
Felix AKN, Martins JJ, Almeida JGL, Giro MEA, Cavalcante KF, Melo VMM, Pessoa ODL, Rocha MVP, Gonçalvez LRB, Aguiar RS (2019) Purification and characterization of a biosurfactant produced by Bacillus subtilis in cashew apple juice and its application in the remediation of oil-contaminated soil. Colloids Surf B 175:256–263. https://doi.org/10.1016/j.colsurfb.2018.11.062
Fontes GC, Ramos NM, Amaral PFF, Nele M, Coelho MAZ (2012) Renewable resources for biosurfactant production by Yarrowia lipolytica. Braz J Chem Eng 29:483–494. https://doi.org/10.1590/S0104-66322012000300005
Guarino C, Spada V, Sciarrillo R (2017) Assessment of three approaches of bioremediation (natural attenuation, landfarming and bioagumentation—assistited landfarming) for a petroleum hydrocarbons contaminated soil. Chemosphere 170:10–16. https://doi.org/10.1016/j.chemosphere.2016.11.165
Hassan M, Essam T, Yassin AS, Salama A (2016) Optimization of rhamnolipid production by biodegrading bacterial isolates using Plackett–Burman design. Int J Biol Macromol 82:573–579. https://doi.org/10.1016/j.ijbiomac.2015.09.057
Jemil N, Hmidet N, Ayed HB, Nasri M (2018) Physicochemical characterization of Enterobacter cloacae C3 lipopeptides and their applications in enhancing diesel oil biodegradation. Process Saf Environ Prot 117:399–407. https://doi.org/10.1016/j.psep.2018.05.018
Karlapudi AP, Venkateswarulu TC, Tammineedi J, Kanumuri L, Ravuru BK, Dirisala VR, Kodali VP (2018) Role of biosurfactants in bioremediation of oil pollution-a review. Petroleum 4:241–249. https://doi.org/10.1016/j.petlm.2018.03.007
Kim SJ, Choi DH, Sim DS, Oh YS (2005) Evaluation of bioremediation effectiveness on crude oil-contaminated sand. Chemosphere 59:845–852. https://doi.org/10.1016/j.chemosphere.2004.10.058
Kim DH, Hwang BR, Moon DH, Kim YS, Baek K (2013) Environmental assessment on a soil washing process of a Pb-contaminated shooting range site: a case study. Environ Sci Pollut Res 20:8417–8424. https://doi.org/10.1007/s11356-013-1599-8
Klis FM, Mol P, Hellingwerf K, Brul S (2002) Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol Rev 26:239–256. https://doi.org/10.1111/j.1574-6976.2002.tb00613.x
Kreling NE, Zaparoli M, Rodigueri G, Colla LM (2015) Produção de biossurfactantes intra e extracelulares a partir de Saccharomyces cerevisiae. https://proceedings.science/sinaferm/sinaferm-2015/papers/producao-de-biossurfactantes-intra-e-extracelulares-a-partir-de-saccharomyces-cerevisiae?lang=pt-br. Accessed 28 Nov 2018
Kreling NE, Zaparoli M, Cecchin I, Thomé A, Reddy KR, Colla LM (2018) Inactive yeast biomass and mannoproteins influence the retention and biodegradation of biodiesel in soil. Environ Qual Manag 28:105–112. https://doi.org/10.1002/tqem.21590
Larik IA, Qazi MA, Phulpoto AH, Haleem A, Ahmed S, Kanhar NA (2019) Stenotrophomonas maltophilia strain 5DMD: an efficient biosurfactant-producing bacterium for biodegradation of diesel oil and used engine oil. Int J Environ Sci Technol 16:259–268. https://doi.org/10.1007/s13762-018-1666-2
Lin L, Cunshan Z, Vittayapadung S, Xiangqian S, Mingdong D (2011) Opportunities and challenges for biodiesel fuel. Appl Energy 88:1020–1031. https://doi.org/10.1016/j.apenergy.2010.09.029
Liu XY, Wang Q, Cui SW, Liu HZ (2008) A new isolation method of β-D-glucans from spent yeast Saccharomyces cerevisiae. Food Hydrocoll 22:239–247. https://doi.org/10.1016/j.foodhyd.2006.11.008
Liu Y, Koh CMJ, Ji L (2011) Bioconversion of crude glycerol to glycolipids in Ustilago maydis. Bioresour Technol 102:3927–3933. https://doi.org/10.1016/j.biortech.2010.11.115
Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem Int J 22:2280–2292. https://doi.org/10.1590/S1516-89132009000200004
Melo ANF, Souza EL, Silva VB, Magnani M (2015) Stability, nutritional and sensory characteristics of French salad dressing made with mannoprotein from spent brewer’s yeast. LWT Food Sci Technol 62:771–774. https://doi.org/10.1016/j.lwt.2014.06.050
Meneghetti L (2007) Biorremediação na descontaminação de um solo residual de basalto contaminado com óleo diesel e biodiesel. Dissertation, University of Passo Fundo
Meyer DD, Beker SA, Bücker F, Peralba MDCR, Frazzon APG, Osti JF, Andreazza R, Camargo FAO, Bento FM (2014) Bioremediation strategies for diesel and biodiesel in oxisol from southern Brazil. Int Biodeterior Biodegrad 95:356–363. https://doi.org/10.1016/j.ibiod.2014.01.026
Morais RK, Abud AKS (2012) Utilização de biossurfactantes produzidos a partir de resíduos agroindustriais na biorremediação do petróleo. Sci Plena 8:1–7
Nelson DL, Cox MM (2014) Princípios de Bioquímica de Lehninger. Artmed, São Paulo
Nievas ML, Commendatore MG, Esteves JL, Bucalá V (2008) Biodegradation pattern of hydrocarbons from a fuel oil-type complex residue by an emulsifier-producing microbial consortium. J Hazard Mater 154:96–104. https://doi.org/10.1016/j.jhazmat.2007.09.112
Oliveira SJ, Antoniassi R, Freitas SC, Müller MD (2013) Composição química da glicerina produzida por usinas de biodiesel no Brasil e potencial de uso na alimentação animal. Cien Rural 43:509–512. https://doi.org/10.1590/S0103-84782013000300022
Pacheco GJ, Ciapina EMP, Gomes EDB, Pereira Junior N (2010) Biosurfactant production by Rhodococcus erythropolis and its application to oil removal. Braz J Microbiol 41:685–693. https://doi.org/10.1590/S1517-83822010000300019
Pareilleux A (1979) Hydrocarbon assimilation by Candida lipolytica: formation of a biosurfactant; effects on respiratory activity and growth. Eur J Appl Microbiol Biotechnol 8:91–101. https://doi.org/10.1007/BF00510270
Reddy KR, Adams JA (2015) Sustainable remediation of contaminated sites. Momentum Press, New York
Roy A, Dutta A, Pal S, Gupta A, Sarkar J, Chatterjee A, Saha A, Sarkar P, Sar P, Kazy S (2018) Biostimulation and bioaugmentation of native microbial community accelerated bioremediation of oil refinery sludge. Bioresour Technol 253:22–32. https://doi.org/10.1016/j.biortech.2018.01.004
Rufino RD, Luna JM, Takaki GMC, Sarubbo LA (2014) Characterization and properties of the biosurfactant produced by Candida lipolytica UCP 0988. Electron J Biotechnol 17:34–38. https://doi.org/10.1016/j.ejbt.2013.12.006
Saharan BS, Sahu RK, Sharma D (2011) A review on biosurfactants: fermentation, current developments and perspectives. Genet Eng Biotechnol J 2011:1–14
Santos DK, Brandão YB, Rufino RD, Luna JM, Salgueiro AA, Santos VA, Sarubbo LA (2014) Optimization of cultural conditions for biosurfactant production from Candida lipolytica. Biocatal Agric Biotechnol 3:48–57. https://doi.org/10.1016/j.bcab.2014.02.004
Santos DKF, Meira HM, Rufino RD, Luna JM, Sarubbo LA (2017) Biosurfactant production from Candida lipolytica in bioreactor and evaluation of its toxicity for application as a bioremediation agent. Process Biochem 54:20–27. https://doi.org/10.1016/j.procbio.2016.12.020
Satpute SK, Banpurkar AG, Dhakephalkar PK, Banat IM, Chopade BA (2010) Methods for investigating biosurfactants and bioemulsifiers: a review. Crit Rev Biotechnol 30:127–144. https://doi.org/10.3109/07388550903427280
Silva DP, Pessoa A, Roberto IC, Vitolo M (2001) Effect of agitation and aeration on production of hexokinase by Saccharomyces cerevisiae. Appl Biochem Biotechnol 91:605–613. https://doi.org/10.1007/978-1-4612-0217-2_51
Silva SNRL, Farias CBB, Rufino RD, Luna JM, Sarubbo LA (2010) Glycerol as substrate for the production of biosurfactant by Pseudomonas aeruginosa UCP0992. Colloids Surf B 79:174–183. https://doi.org/10.1016/j.colsurfb.2010.03.050
Sousa MD, Dantas IT, Felix AKN, Sant’Ana HBD, Melo VMM, Gonçalves LRB (2014) Crude glycerol from biodiesel industry as substrate for biosurfactant production by Bacillus subtilis ATCC 6633. Braz Arch Biol Technol 57:295–301. https://doi.org/10.1590/S1516-89132014000200019
Streck EV (2008) Solos do Rio Grande do Sul. Emater, Porto Alegre
Teixeira AS (2007) Isolamento e caracterização de bactérias degradadoras de gasolina comercial. Dissertation, Federal University of Rio Grande do Sul
Thomé A, Reginatto C, Cecchin I, Colla LM (2014) Bioventing in a residual clayey soil contaminated with a blend of biodiesel and diesel oil. J Environ Eng 140:1–6. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000863
Tininis CRCS Gattas EADL (2002) Efeito da temperatura de estocagem de leveduras de panificação sobre a atividade da glicerol-3-fosfato desidrogenase. Rev Bras Ciênc Farm 38:81–87. https://doi.org/10.1590/S1516-93322002000100008
Usepa, Environmental Protection Agency (1996) Method 3550B: ultrassonic extraction. http://www.trincoll.edu/~henderso/textfi~1/416%20notes/3550b.pdf. Accessed 15 Sept 2015
Vyas TK, Dave BP (2011) Production of biosurfactant by Nocardia otitidiscaviarum and its role in biodegradation of crude oil. Int J Environ Sci Technol 8:425–432. https://doi.org/10.1007/BF03326229
Weber L, Döge C, Haufe G, Hommel R, Kleber HP (1992) Oxygenation of hexadecane in the biosynthesis of cyclic glycolipids in Torulopsis apicola. Biocatalysis 5:267–272. https://doi.org/10.3109/10242429209014872
Win SS, Impoolsup A, Noomhorm A (1996) Growth kinetics of Saccharomyces cerevisiae in batch and fedbatch cultivation using sugarcane molasses and glucose syrup from cassava starch. J Ind Microbiol 16:117–123. https://doi.org/10.1007/BF01570071
Yaron B, Dror I, Berkowitz B (2008) Soil-subsurface change: chemical pollutant impacts. Springer, Berlin
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We acknowledge that the authors are thankful to Coordination of Improvement of Higher Level Personnel (CAPES, National Council for Scientific and Technological Development (CNPq)) and University of Passo Fundo for financing and support.
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Kreling, N.E., Zaparoli, M., Margarites, A.C. et al. Extracellular biosurfactants from yeast and soil–biodiesel interactions during bioremediation. Int. J. Environ. Sci. Technol. 17, 395–408 (2020). https://doi.org/10.1007/s13762-019-02462-9
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DOI: https://doi.org/10.1007/s13762-019-02462-9