Abstract
We aimed to produce simultaneously biosurfactants and lipases in solid state fermentation (SSF) using Aspergillus niger, followed by the use of the fermented media on the bioremediation of oily contaminated soil, in order to valuate agro industrial residuals and reduce the contamination. The biocompounds were produced using wheat bran and corncob (80:20), 5% of soybean oil and 0.5% of sugar cane molasses in SSF for 4 d, producing 4.58 ± 0.69 UE of emulsifying activity and 7.77 ± 1.52 U of lipolytic activity. This fermented media was used in the bioremediation of a 20% biodiesel contaminated soil, evaluating for 90 d microbial growth, contaminant degradation, and production of lipases and biosurfactants in soils. Six experimental strategies (natural attenuation; biostimulation + bioaugmentation + biocompounds; biostimulation + biosurfactant; biocompounds extract; biostimulation; adsorption of contaminant) were realized. The highest degradation of contaminant was verified in 90 d, of 74.40 ± 1.76%, and the production of biosurfactants and lipases in situ in the soil was found in 30 d (6.02 ± 0.24% of reduction in surface tension and 6.62 ± 0.17 UL of lipid activity in soil) for the same experiment (biostimulation + bioaugmentation + biocompounds). The addition of biostimulation + biosurfactant promotes higher biodegradation (66.00 ± 0.92%) of the contaminant than the biocompounds extract (59.58 ± 0.34%). The use of a solid fermented culture medium containing both biocompounds was feasible for the treatment of contaminants, demonstrating the potential for environmental application without the need for purification processes.
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References
Ángeles MT, Refugio RV (2013) In situ biosurfactant production and hydrocarbon removal by Pseudomonas putida CB-100 in bioaugmented and biostimulated oil contaminated soil. Braz J Microbiol 44:595–605. https://doi.org/10.1590/s1517-83822013000200040
American Society for Testing and Materials (2013) . Standard Specification for Woven Wire Test Sieve Cloth and Test Sieves. ASTM E11 - 13, West Conshohocken, United States
Bento FM, Camargo FAO, Okeke BC, Frankenberger WT (2005) Comparative bioremediation of soils contaminated with diesel oil by natural attenuation, biostimulation and bioaugmentation. Bioresour technol 96:1049–1055. https://doi.org/10.1016/j.biortech.2004.09.008
Berg JM, Tymoczko JL, Stryer L (2006) Biochemistry: International edition. W. H. Freeman, New York, NY
Brasil (2003a). Official analytical methods for microbiological analyzes for the 478 control of animal products and water - Chapter I: Standard count of mesophilic aerobic strict 479 and facultative viable microorganisms. Official Diary of the Union (in Portuguese). https://www.defesa.agricultura.sp.gov.br/legislacoes/instrucao-normativa-sda-62-de-26-08-2003,665.html. Accessed 26 March 2020
Brasil (2018) Resolution n°16, 29 October 2018. Official Diary of the Union http://www.mme.gov.br/documents/36074/265770/Resolucao_16_CNPE_29-10-18.pdf/03661cf7-007d-eb99-10b4-61ee59c30941. Accessed 26 March 2020. (in Portuguese)
Burkert JFM, Maugeri F, Rodrigues MI (2004) Optimization of extracellular lipase production by Geotrichum sp. using factorial design. Bioresour Technol 91:77–84. https://doi.org/10.1016/S0960-8524(03)00152-4
Castiglioni GL, Bertolin TE, Costa JAV (2009) Solid-state biosurfactant production by Aspergillus fumigatus using agricultural residues as substrate. Quim Nova 32:292–295. https://doi.org/10.1590/S0100-40422009000200005
Cavka A, Alriksson B, Rose SH, Van zyl WH, Jönsson LJ (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 41:1191–1200. https://doi.org/10.1007/s10295-014-1457-9
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 142:04015093–04015093-8. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001060
Chaprão MJ, Ferreira INS, Correa PF, Rufino RD, Luna JM, Silva EJ, Sarubbo LA (2015) Application of bacterial and yeast biosurfactants for enhanced removal and biodegradation of motor oil from contaminated sand. Electron J Biotechnol 18:471–479. https://doi.org/10.1016/j.ejbt.2015.09.005
Chikere CB, Tekere M, Adeleke R (2019) Enhanced microbial hydrocarbon biodegradation as stimulated during field-scale landfarming of crude oil-impacted soil. Sustain Chem Pharm 14:100177. https://doi.org/10.1016/j.scp.2019.100177
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
Colla LM, Rizzardi J, Pinto MH, Reinehr CO, Bertolin TE, Costa JAV (2010) Simultaneous production of lipases and biosurfactants by submerged and solid-state bioprocesses. Bioresour Technol 101:8308–8314. https://doi.org/10.1016/j.biortech.2010.05.086
Cetesb (2018) Report of contaminated and rehabilitated areas in the state of São Paulo. Environmental Company of the State of São Paulo. https://cetesb.sp.gov.br/areas-contaminadas/wp-content/uploads/sites/17/2020/02/TEXTO-EXPLICATIVO-2019-12.02.20.pdf. Accessed 22 March 2020
Contesini FJ, Lopes DB, Macedo GA, Nascimento MG, Carvalho PO (2010) Aspergillus sp. lipase: potential biocatalyst for industrial use. J Mol Catal B Enzym 67:163–171
Cooper DG, Goldenberg BG (1987) Surface-active agents from two Bacillus species. Appl Environ Microbiol 53:224–229. https://doi.org/10.1016/j.molcatb.2010.07.021
Decesaro A, Berticelli R, Magro FG, Colla LM (2015) Biossurfactantes em Processos de Biorremediação. Rev Cienc Exatas Nat 17:121–145. https://doi.org/10.5935/RECEN.2015.01.06
Decesaro A, Rempel A, Machado TS, Cappellaro, AC, Machado BS, Cechin I, Thomé A, Colla LM (2021) Bacterial biosurfactant increases ex situ biodiesel bioremediation in clayey soil. Biodegradation 1–13. https://doi.org/10.1007/s10532-021-09944-z
Decesaro A, Rempel A, Machado TS, Thomé A, Reddy K, Margarites AC, Colla LM (2016) Bioremediation of soil contaminated with diesel and biodiesel fuel using biostimulation with microalgae biomass. J Environ Eng 143:04016091. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001165
Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64. 0146-0749/97/$04.0010
Devaraj S, Sabapathy PC, Nehru L, Preethi K (2019) Bioprocess optimization and production of biosurfactant from an unexplored substrate: Parthenium hysterophorus. Biodegradation 30:325–334. https://doi.org/10.1007/s10532-019-09878-7
Fleuri LF, Oliveira MC, Arcuri MLC, Capoville BL, Pereira MS, Delgado CHO, Novelli PK (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 23:1199–1205. https://doi.org/10.1007/s10068-014-0164-7
Fontes GC, Amaral PFF, Coelho MAZ (2008) Yeast biosurfactant production. Quím Nova 31:2091–2099. https://doi.org/10.1590/S0100-40422008000800033. (in Portuguese)
Gupta PK (2020) Fate, transport, and bioremediation of biodiesel and blended biodiesel in subsurface environment: a review. J Environ Eng 146:1–10. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001619
Herrero M, Stuckey DC (2015) Bioaugmentation and its application in wastewater treatment: a review. Chemosphere 140:119–128. https://doi.org/10.1016/j.chemosphere.2014.10.033
Huang Y, Zhou H, Zheng G, Li Y, Xie Q, You S, Zhang C (2020) Isolation and characterization of biosurfactant-producing Serratia marcescens ZCF25 from oil sludge and application to bioremediation. Environ Sci Pollut Res 27:27762–27772. https://doi.org/10.1007/s11356-020-09006-6
Kim D, Hwang B, Moon D, Kim Y, 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
Kiran S, Arshad Z, Nosheen S, Kamal S, Gulzar T, Majeed MS, Jannat M, Rafique MA (2016) Microbial lipases: production and applications: a review. J Biochem Biotechnol Biomat 1:7–20
Kreling NE, Zaparoli M, Margarites AC, Friedrich MT, Thomé A, Colla LM (2019) Extracellular biosurfactants from yeast and soil – biodiesel interactions during bioremediation. Int J Environ Sci Technol 17:395–408. https://doi.org/10.1007/s13762-019-02462-9
Kreling NE, Simon V, Fagundes VD, Thomé A, Colla LM (2020) Simultaneous production of lipases and biosurfactants in solid-state fermentation and use in bioremediation. J Environ Eng 146:04020105–04020105. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001785
Kumar DS, Ray S (2014) Fungal lipase production by solid state fermentation-an overview. J Anal Bioanal Tech 6:1–10. https://doi.org/10.4172/2155-9872.1000230
Kumar S, Mathur A, Singh V, Nandy S, Khare SK (2012) Bioremediation of waste cooking oil using a novel lipase produced by Penicillium chrysogenum SNP5 grown in solid medium containing waste grease. Bioresour Technol 120:300–304. https://doi.org/10.1016/j.biortech.2012.06.018
Lin X, Li X, Sun T, Li P, Zhou Q, Sun L, Hu X (2009) Changes in microbial populations and enzyme activities during the bioremediation of oil-contaminated soil. Bull Environ Contam Toxicol 83:542–547. https://doi.org/10.1007/s00128-009-9838-x
Machado TS, Decesaro A, Capellaro AC, Machado BS, Reginato KVS, Reinehr CO, Thomé A, Colla LM (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
Mahmoud GA, Koutb MMM, Morsy FM, Bagy MMK (2015) Characterization of lipase enzyme produced by hydrocarbons utilizing fungus Aspergillus terreus. Eur J Biol Res 5:70–77
Makkar RS, Rockne KJ (2003) Comparison of synthetic surfactants and biosurfactants in enhancing biodegradation of polycyclic aromatic hydrocarbons. Environ Toxicol Chem 22:2280–2292. https://doi.org/10.1897/02-472
Maletić SP, Beljin JM, Roncevic SD, Grgic MC, Dalmacija BD (2019) State of the art and future challenges for polycyclic aromatic hydrocarbons is sediments: sources, fate, bioavailability and remediation techniques. J Hazard Mater 365:467–482. https://doi.org/10.1016/j.jhazmat.2018.11.020
Margesin R, Zimmerbauer A, Schinner F (1999) Soil lipase activity–a useful indicator of oil biodegradation. Biotechnol Tech 13:859–863. https://doi.org/10.1023/A:1008928308695
Martins VG, Kalil SJ, Costa JAV (2008) Co-production of lipase and biosurfactant in solid state for use in bioremediation of vegetable oils and hydrocarbons. Quím Nova 31:942–1947. https://doi.org/10.1590/S0100-40422008000800005. (in Portuguese)
Meneghetti L (2007). Bioremediation in the decontamination of a residual basalt soil contaminated with diesel oil and biodiesel. Dissertation, University of Passo Fundo (in Portuguese)
Meyer DD, Beker AA, Bucker F, Peralba MCR, 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
Mulligan CN (2009) Recent advances in the environmental applications of biosurfactants. Curr Opin Colloid Interface Sci 14:372–378. https://doi.org/10.1016/j.cocis.2009.06.005
Nievas ML, Commendatore JL, Esteves VB (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
Olajuyigbe FM, Adeleye OA, Kolawole AO, Bolarinwa TO, Fasakin EA, Asenuga ER, Ajele JO (2020) Bioremediation treatment improves water quality for Nile tilapia (Oreochromis niloticus) under crude oil pollution. Environ Sci Pollut Res 27:25689–25702. https://doi.org/10.1007/s11356-020-09020-8
Ossai IC, Ahmed A, Hassan A, Hamid FS (2019) Remediation of soil and water contaminated with petroleum hydrocarbon: a review. Environ Technol Innov 17:100526. https://doi.org/10.1016/j.eti.2019.100526
Pacwa-Płociniczak M, Plaza GA, Piotrowska-Seget Z, Cameotra SS (2011) Environmental applications of biosurfactants: recent advances. Int J Mol Sci 12:633–654. https://doi.org/10.3390/ijms12010633
Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84. https://doi.org/10.1016/S1369-703X(02)00121-3
Perfumo A, Banat IM, Marchant R (2018) Going green and cold: biosurfactants from low-temperature environments to biotechnology applications. Trends Biotechnol 36:277–289. https://doi.org/10.1016/j.tibtech.2017.10.016
Quintella CM, Mata AMT, Lima LCP (2009) Overview of bioremediation with technology assessment and emphasis on fungal bioremediation of oil contaminated soils. J Environ Manag 241:156–166. https://doi.org/10.1016/j.jenvman.2019.04.019
Reddy KR, Adams JA (2015) Sustainable remediation of contaminated sites. Momentum Press, New York, NY
Reinehr CO, Treichel H, Tres MV, Steffens J, Brião VB, Colla LM (2017) Successive membrane separation processes simplify concentration of lipases produced by Aspergillus niger by solid-state fermentation. Bioprocess Biosyst Eng 40:843–855. https://doi.org/10.1007/s00449-017-1749-3
Rodrigues EF, Reinehr CO, Bertolin TE, Colla LM (2014) Production of compounds with emulsifying properties by Aspergillus flavus using agro-industrial waste. Exact Nat Sci J 18:97–115. https://doi.org/10.5935/RECEN.2016.01.05. in Portuguese
Salgado JM, Abrunhosa L, Venâncio A, Domínguez JM, Belo I (2016) Combined bioremediation and enzyme production by Aspergillus sp. in olive mill and winery wastewaters. Int Biodeterior Biodegrad 110:16–23. https://doi.org/10.1016/j.ibiod.2015.12.011
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
Sena HH, Sanches MA, Rocha DFS, Segundo WOPF, Souza ES, Souza JVB (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
Shaheen SM, Antoniadisd V, Kwone E, Songe H, Wangf S, Hseuf Z, Rinklebea J (2020) Soil contamination by potentially toxic elements and the associated human health risk in geo-and anthropogenic contaminated soils: a case study from the temperate region (Germany) and the arid regions (Egypt). Environ Pollut 114312. https://doi.org/10.1016/j.envpol.2020.114312
Sharma A, Kumar P, Rehman MB (2014) Biodegradation of diesel hydrocarbon in soil by bioaugmentation of Pseudomonas aeruginosa: a laboratory scale study. Int J Environ Biorem Biodegrad 2:202–212. https://doi.org/10.12691/ijebb-2-4-8
Silva RCF, Almeida DG, Brasileiro PPF, Rufino RD, Luna JM, Sarubbo LA (2019) Production, formulation and cost estimation of a commercial biosurfactant. Biodegradation 30:191–201. https://doi.org/10.1007/s10532-018-9830-4
Singh D, Sharma D, Soni SL, Sharma S, Sharma PK, Jhalani A (2020) A review on feedstocks, production processes, and yield for different generations of biodiesel. Fuel 262:116553. https://doi.org/10.1016/j.fuel.2019.116553
Soccol CR, Costa ESF, Letti LAJ, Karp SG, Woiciechowski AL, Vandenberghe LPS (2017) Recent developments and innovations in solid state fermentation. Biotechnol Res Innov 1:52–71. https://doi.org/10.1016/j.biori.2017.01.002
Sperb JGC, Costa TM, Vaz DA, Valle JAB, Valle RCSC, Tavares LBB (2015) Qualitative evaluation of the production of lipases and biosurfactants by fungi isolated from oily residues. Engevista 17:385–397. https://doi.org/10.22409/engevista.v17i3.690. (in Portuguese)
Streck EV (2008) Soils of Rio Grande do Sul. EMATER/RS, Brazil (in Portuguese)
Teixeira AS (2007) Isolation and characterization of commercial gasoline-degrading bacteria. Dissertation, Federal University of Rio Grande do Sul (in Portuguese)
Thomé A, Reginatto C, Checchin I, Colla LM (2014) Bioventing in a residual clayey soil contaminated with a blend of biodiesel and diesel oil. J Environ Eng 140:06014005–06014005. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000863
Urum K, Pekdemir T (2004) Evaluation of biosurfactants for crude oil contaminated soil whashing. Chemosphere 57:1139–1150. https://doi.org/10.1016/j.chemosphere.2004.07.048
USEPA (1996) Method 3550B: Ultrassonic Extraction. http://www.trincoll.edu/~henderso/textfi~1/416%20notes/3550b.pdf. Accessed 05 Aug 2020
Utami TS, Hariyani I, Alamsyah G, Hermansyah H (2017) Production of dry extract extracellular lipase from Aspergillus niger by solid state fermentation method to catalyze biodiesel synthesis. Energy Procedia 136:41–46. https://doi.org/10.1016/j.egypro.2017.10.275
Uzoigwe C, Burgess JG, Ennis CJ, Rahman PKSM (2015) Bioemulsifiers are not biosurfactants and require different screening approaches. Front Microbiol 6:1–6. https://doi.org/10.3389/fmicb.2015.00245
Yalaoui-Guellal D, Fella-Temzi S, Djafri-Dib S, Brahmi F, Banat IM, Madani K (2020) Biodegradation potential of crude petroleum by hydrocarbonoclastic bacteria isolated from Soummam wadi sediment and chemical-biological proprieties of their biosurfactants. J Pet Sci Eng 184:106554. https://doi.org/10.1016/j.petrol.2019.106554
Acknowledgements
The authors thank the National Council for Scientific and Technological Development (CNPq) for the financial support, project number 408866/2016-0, Rio Grande do Sul State Research Support Foundation (FAPERGS), BS Bios company for supplying the biodiesel used in this work and University of Passo Fundo.
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This study was funded by National Council for Scientific and Technological Development (CNPq), project number 408866/2016-0 and FAPEGRS and Rio Grande do Sul State Research Support Foundation (FAPERGS).
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by NEK, VS, and VDF. The first draft of the manuscript was written by NEK, LMC, and AT, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Kreling, N.E., Simon, V., Fagundes, V.D. et al. Improving the Bioremediation and in situ Production of Biocompounds of a Biodiesel-Contaminated Soil. Environmental Management 68, 210–225 (2021). https://doi.org/10.1007/s00267-021-01486-7
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DOI: https://doi.org/10.1007/s00267-021-01486-7