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Application of rhamnolipid surfactant for remediation of toxic metals of long- and short-term contamination sites

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Abstract

A rhamnolipid extract from Pseudomonas aeruginosa was tested on soils from short- and long-term contamination sites. Mass spectrometry analysis revealed a predominance of di-rhamnolipid congeners (85%), of which hydroxydecanoyl-hydroxydecanoate was the most abundant. Artificial contamination of a sandy soil resulted in final concentrations of arsenic, cadmium and zinc of 182, 20 and 983 mg kg−1, respectively. The rhamnolipid showed a high extractive capacity for transition metals and metalloids, removing 53% of the arsenic, 90% of the cadmium and 80% of the zinc from the artificially contaminated soil. When tested against soil samples from a deactivated mining site, the rhamnolipid removed 59% of the arsenic, 57% of cadmium and 9% of zinc. The biosurfactant showed excellent biocompatibility with Artemia salina. Well diffusion tests demonstrated that the rhamnolipid was innocuous for commensally soil bacteria and yeast. A method for precipitation of As, Cd and Zn was tested to allow eco-friendly disposal of these metal(loid) contaminants. The precipitation method was able to remove all the arsenic and cadmium, while removing 84.5% of zinc in the biosurfactant solution. The possibility of applying this biosurfactant to soil remediation processes without purification steps and the development of new and rapid methods for metal precipitation are strategically important for the mining industry, to properly dispose or recycle metal contaminants and thus reduce the demand for new raw materials.

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References

  • Abdel-Mawgoud AM, Lépine F, Déziel E (2010) Rhamnolipids: diversity of structures, microbial origins and roles. Appl Microbiol Biotech 86:1323–1336. https://doi.org/10.1007/s00253-010-2498-2

    Article  CAS  Google Scholar 

  • Alves W, Ferreira P, Colombo CR, Portela CR (2017) Environmental strategies for the mining sector: evidences from a Brazilian company. REBRAE Rev Bras Estratégia 10:186–220

    Google Scholar 

  • Appel C, Ma L (2002) Concentration, pH, and surface charge effects on cadmium and lead sorption in three tropical soils. J Environ Qual 31:581–589

    CAS  Google Scholar 

  • Aşçi Y, Nurbaş M, Açikel YS (2008) A comparative study for the sorption of Cd(II) by soils with different clay contents and mineralogy and the recovery of Cd(II) using rhamnolipid biosurfactant. J Hazard Mater 154:663–673. https://doi.org/10.1016/j.jhazmat.2007.10.078

    Article  CAS  Google Scholar 

  • Behrens B, Baune M, Jungkeit J, Tiso T, Blank LM, Hayen H (2016) High performance liquid chromatography-charged aerosol detection applying an inverse gradient for quantification of rhamnolipid biosurfactants. J Chromatogr A 1455:125–132. https://doi.org/10.1016/j.chroma.2016.05.079

    Article  CAS  Google Scholar 

  • Casla D, Requena T, Gómez R (1996) Antimicrobial activity of lactic acid bacteria isolated from goat’s milk and artisanal cheeses: characteristics of a bacteriocin produced by Lactobacillus curvatus IFPL105. J Appl Bacteriol 81:35–41. https://doi.org/10.1111/j.1365-2672.1996.tb03279.x

    Article  CAS  Google Scholar 

  • Chen M, Dong C, Penfold J, Thomas RK, Smyth TJP, Perfumo A, Marchant R et al (2013) Influence of calcium ions on rhamnolipid and rhamnolipid/anionic surfactant adsorption and self-assembly. Langmuir 29:3912–3923. https://doi.org/10.1021/la400432v

    Article  CAS  Google Scholar 

  • Chen W, Qu Y, Xu Z, He F, Chen Z, Huang S, Li Y (2017) Heavy metal (Cu, Cd, Pb, Cr) washing from river sediment using biosurfactant rhamnolipid. Environ Sci Pollut Res 24:16344–16350

    CAS  Google Scholar 

  • CLSI – Clinical and Laboratory Standards Institute (2016) M23-A4. Development of in vitro susceptibility testing criteria and quality control parameters, 4th ed. Clinical and Laboratory Standards Institute, Wayne, PA

  • Cotou E, Castritsi-Catharios I, Moraitou-Apostolopoulou M (2001) Surfactant-based oil dispersant toxicity to developing nauplii of Artemia: effects on ATPase enzymatic system. Chemosphere 42:959–964

    CAS  Google Scholar 

  • Crawford RJ, Harding IH, Mainwaring DE (1993) Adsorption and coprecipitation of single heavy metal ions onto the hydrated oxides of iron and chromium. Langmuir 9:3050–3056

    CAS  Google Scholar 

  • da Rocha Junior RB, Meira HM, Almeida DG, Rufino RD, Luna JM, Santos VA, Sarubbo LA (2018) Application of a low-cost biosurfactant in heavy metal remediation processes. Biodegradation 30:2015–2233. https://doi.org/10.1007/s10532-018-9833-1

    Article  CAS  Google Scholar 

  • da Silva EB, de Oliveira LM, Wilkie AC, Liu Y, Ma LQ (2018) Arsenic removal fromAs-hyperaccumulator Pteris vittata biomass: Coupling extraction with precipitation. Chemosphere 193:288–294

    Google Scholar 

  • Déziel E, Lépine F, Milot S, Villemur R (2000) Mass spectrometry monitoring of rhamnolipids from a growing culture of Pseudomonas aeruginosa strain 57RP. Biochim Biophys Acta (BBA)-MolCell BiolLipids 1485:145–152

    Google Scholar 

  • Déziel E, Lepine F, Milot S, Villemur R (2003) rhlA is required for the production of a novel biosurfactant promoting swarming motility in Pseudomonas aeruginosa: 3-(3-hydroxyalkanoyloxy) alkanoic acids (HAAs), the precursors of rhamnolipids. Microbiology 149:2005–2013

    Google Scholar 

  • do Carmo FF, Kamino LHY, Tobias Junior R, de Campos IC, do Carmo FF, Silvino G, de Castro KJDX, Mauro ML, Rodrigues NUA, Miranda MP, de Souza PCEF (2017) Fundão tailings dam failures: the environment tragedy of the largest technological disaster of Brazilian mining in global context. Perspect Ecol Conserv 15:145–151. https://doi.org/10.1016/j.pecon.2017.06.002

    Article  Google Scholar 

  • Empresa Brasileira de Pesquisa Agropecuária – EMBRAPA (1997) Manual de métodos de análise de solo, 2nd ed. Centro Nacional de Pesquisas de Solos, Rio de Janeiro, Brazil. https://www.agencia.cnptia.embrapa.br/Repositorio/Manual+de+Metodos_000fzvhotqk02wx5ok0q43a0ram31wtr.pdf. Accessed 20 Aug 2018

  • European Economic Community – EEC (2019) European Union Directive No. 67/548/EEC, 1967. http://aei.pitt.edu/3331/1/3331.pdf. Accessed 12 Jul 2019

  • Fernandes GW, Goulart FF, Ranieri BD, Coelho MS, Dales K, Boesche N, Bustamante M, Carvalho FA et al (2016) Deep into the mud: ecological and socio-economic impacts of the dam breach in Mariana, Brazil. NatConserv 14:35–45

    Google Scholar 

  • Ferreira Fontes MP, de Matos AT, da Costa LM, Lima Neves JC (2000) Competitive adsorption of zinc, cadmium, copper, and lead in three highly-weathered Brazilian soils. Comm Soil Sci Plant Anal 31:2939–2958

    Google Scholar 

  • Finney DJ (1949) The adjustment for anatural response rate in probitanalysis. Ann Appl Biol 36:187–195. https://doi.org/10.1111/j.1744-7348.1949.tb06408.x

    Article  CAS  Google Scholar 

  • Gotschol A, De Giovanni P, Vinzi VE (2014) Is environmental management an economically sustainable business? J Environ Manag 144:73–82

    Google Scholar 

  • Habba E, Pinazo A, Jáuregui O, Espuny MJ, Infante MR, Manresa A (2003) Physicochemical characterization and antimicrobial properties of rhamnolipids produced by Pseudomonas aeruginosa 47T2 NCBIM 40044. Biotech Bioeng 81:316–322

    Google Scholar 

  • Henkel M, Müller MM, Kügler JH, Lovaglio RB, Contiero J, Syldatk C, Hausmann R (2012) Rhamnolipids as biosurfactants from renewable resources: concepts for next-generation rhamnolipid production. Process Biochem 47:1207–1219

    CAS  Google Scholar 

  • Herman DC, Artiola JF, Miller RM (1995) Removal of cadmium, lead, and zinc from soil by a rhamnolipid biosurfactant. Environ Sci Technol 29:2280–2285

    CAS  Google Scholar 

  • Honna CY (2013) Obtenção e análise de mutantes de Pseudomonas aeruginosa afetados na biossíntese de ramnolipídeos. Dissertation, Universidade de São Paulo. https://doi.org/10.11606/D.42.2013.tde-26062014-112650

    Article  Google Scholar 

  • Hubbard AT (2002) Encyclopedia of surface colloid science. CRC Press, Boca Raton

    Google Scholar 

  • Ishigami Y, Gama Y, Ishii F, Choi YK (1993) Colloid chemical effect of polar head moieties of a rhamnolipid-type biosurfactant. Langmuir 9:1634–1636

    CAS  Google Scholar 

  • Johann S, Seiler TB, Tiso T, Bluhm K, Blank LM, Hollert H (2016) Mechanism-specific and whole-organism ecotoxicity of mono-rhamnolipids. Sci Tot Environ 548:155–163

    Google Scholar 

  • Kaya M (2016) Recovery of metals and nonmetals from electronic waste by physical andchemical recycling processes. Waste Manag 57:64–90

    CAS  Google Scholar 

  • Khalid S, Shahid M, Niazi NK, Murtaza B, Bibi I, Dumat C (2017) A comparison of technologies for remediation of heavy metal contaminated soils. J Geo Explor 182:247–268. https://doi.org/10.1016/j.gexplo.2016.11.021

    Article  CAS  Google Scholar 

  • Lee CS, Kao MM (2004) Effects of extracting reagents and metal speciation on the removal of heavy metal contaminated soils by chemical extraction. J Environ Sci Health 39:1233–1249

    Google Scholar 

  • Lenzi E, de Cinque Almeida V, BortottiFavero LO, Juliato Becker F (2011) Detalhes da utilização do íon hidróxido, HO, no tratamento de efluentes contaminados com metal pesado zinco. Acta Sci Technol 33:313–322

    CAS  Google Scholar 

  • Liwarska-Bizukojc E, Miksch K, Malachowska-Jutsz A, Kalka J (2005) Acute toxicity andgenotoxicity of five selected anionic and nonionic surfactants. Chemosphere 58:1249–1253

    CAS  Google Scholar 

  • Luna JM, LA RufinoRD Sarubbo (2016) Biosurfactant from Candida sphaerica UCP0995 exhibiting heavy metal remediation properties. Proc Saf Environ Prot 102:558–566. https://doi.org/10.1016/j.psep.2016.05.010

    Article  CAS  Google Scholar 

  • Magaldi S, Mata-Essayag S, de Capriles HC, Perez C, Colella MT, Olaizola C, Ontiveros Y (2004) Well diffusion for antifungal susceptibility testing. Int J Infect Dis 8:39–45

    CAS  Google Scholar 

  • Mao X, Jiang R, Xiao W, Yu J (2015) Use of surfactants for the remediation of contaminated soils: a review. J Hazard Mater 285:419–435

    CAS  Google Scholar 

  • Martínez CE, Motto HL (2000) Solubility of lead, zinc and copper added to mineral soils. Environ Pollut 107:153–158

    Google Scholar 

  • Monteiro MR, Kugelmeier CL, Pinheiro RS, Batalha MO, da Silva César A (2018) Glycerol from biodiesel production: technological paths for sustainability. Renew Sustain Energ Rev 88:109–122

    CAS  Google Scholar 

  • Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng Geol 60:193–207. https://doi.org/10.1016/S0013-7952(00)00101-0

    Article  Google Scholar 

  • Ochoa-Loza FJ, Artiola JF, Maier RM (2001) Stability constants for the complexation of various metals with a rhamnolipid biosurfactant. J Environ Qual 30:479–485. https://doi.org/10.2134/jeq2001.302479x

    Article  CAS  Google Scholar 

  • Oorts K, Ghesquiere U, Smolders E (2007) Leaching and aging decrease nickel toxicity to soil microbial processes in soils freshly spiked with nickel chloride. Environ Toxicol Chem 26:1130–1138

    CAS  Google Scholar 

  • Papadopoulos P, Rowell DL (1989) The reaction of copper and zinc with calcium carbonate surfaces. J Soil Sci 40:39–48

    CAS  Google Scholar 

  • Park B, Son Y (2017) Ultrasonic and mechanical soil washing processes for the removal of heavy metals from soils. Ultrason Sonochem 35:640–645

    CAS  Google Scholar 

  • PimentelMP Silva-Júnior FCG, Santaella ST, Lotufo LVC (2011) O uso de Artemia sp. comoorganismo-teste para avaliação da toxicidade das águas residuárias do beneficiamento da castanha de caju antes e após tratamento em reator biológico experimental. J Braz Soc Ecol 6:15–22. https://doi.org/10.5132/jbse.2011.01.003

    Article  Google Scholar 

  • Rassaei F, Hoodaji M, Ali Abtahi S (2020) Cadmium fractions in two calcareous soils affected by incubation time, zinc and moisture regime. Commun Soil Sci Plant Anal 51:456–467

    CAS  Google Scholar 

  • Ren ZL, Sivry Y, Tharaud M, CordierL Li Y, Dai J, Benedetti MF (2017) Speciation and reactivity of lead and zinc in heavily and poorly contaminated soils: stable isotope dilution, chemical extraction and model views. EnvironPollut 225:654–662

    CAS  Google Scholar 

  • CONAMA – Conselho Nacional do Meio Ambiente. Resolução no 420, de 28 de dezembro de 2009. Diário Oficial [República Federativa do Brasil], Brasília, DF, no. 249, de 30/12/2009, p 81–84. http://www.mma.gov.br/port/conama/legiano1.cfm?codlegitipo=3&ano=2009. Accessed 20 Aug 2018

  • Sachdev DP, Cameotra SS (2013) Biosurfactants in agriculture. Appl Micro Biotech 97:1005–1016

    CAS  Google Scholar 

  • Saito HE, Harp JR, Fozo EM (2014) Incorporation of exogenous fatty acids protects Enterococcus faecalis from membrane-damaging agents. Appl Environ Microbiol 80:6527–6653. https://doi.org/10.1128/AEM.02044-14

    Article  CAS  Google Scholar 

  • Santos APP, Silva MDS, Costa EVL, Rufino RD, Santos VA, Ramos CS, Sarubbo LA, Porto ALF (2018) Production and characterization of a biosurfactant produced by Streptomyces sp. DPUA 1559 isolated from lichens of the Amazon region. Braz J Med Biol Res 51:e6657

    Google Scholar 

  • Sheppard JD, Mulligan CN (1987) The production of surfactin by Bacillus subtilis grown on peat hydrolysate. Appl Microbiol Biotechnol 27:110–116. https://doi.org/10.1007/BF0025193

    Article  CAS  Google Scholar 

  • Song B, Springer J (1996) Determination of interfacial tension from the profile of a pendant drop using computer-aided image processing: 2. Experimental. J Colloid Interface Sci 184:77–91

    CAS  Google Scholar 

  • Sun L, Chen S, Chao L, Sun T (2007) Effects of flooding on changes in Eh, pH and speciation of cadmium and lead in contaminated soil. Bull Environ Contam Toxicol 79:514–518

    CAS  Google Scholar 

  • Sutherland RA (2010) BCR®-701: a review of 10-years of sequential extraction analyses. Anal Chim Acta 680:10–20

    CAS  Google Scholar 

  • United States Department of Agriculture – USDA Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and interpreting soil surveys, 2nd ed. Natural Resources Conservation Service. U.S. Department of Agriculture Handbook 436. U. S. Government Printing Office, Washington, DC. https://www.nrcs.usda.gov/Internet/FSE_DOCUMENTS/nrcs142p2_051232.pdf. Accessed 20 Jul 2018

  • United States Environmental Protection Agency – USEPA (2007) Method 3051A—microwave assisted acid digestion of sediments, sludges, soils, and oils. https://www.epa.gov/sites/production/files/2015-12/documents/3051a.pdf. Accessed 13 Mar 2018

  • Valgas C, Souza SMD, Smânia EF, Smânia A Jr (2007) Screening methods to determine antibacterial activity of natural products. Braz J Microbiol 38:369–380

    Google Scholar 

  • van Wezel AP, Opperhuizen A (1995) Narcosis due to environmental pollutants in aquatic organisms: residue-based toxicity, mechanisms, and membrane burdens. Crit Rev Toxicol 25:255–279

    Google Scholar 

  • Wang S, Mulligan CN (2004) An evaluation of surfactant foam technology in remediation of contaminated soil. Chemosphere 57:1079–1089

    Google Scholar 

  • Wang S, Mulligan CN (2009) Rhamnolipid biosurfactant-enhanced soil flushing for the removal of arsenic and heavy metals from mine tailings. Process Biochem 44:296–301

    CAS  Google Scholar 

  • Wu J, Zhang J, Wang P, Zhu L, Gao M, Zheng Z, Zhan X (2017) Production of rhamnolipids by semi-solid-state fermentation with Pseudomonas aeruginosa RG18 for heavy metal desorption. Bioprocess Biosyst Eng 40:1611–1619

    CAS  Google Scholar 

  • Zheng SA, Zheng X, Chen C (2012) Leaching behavior of heavy metals and transformation of their speciation in polluted soil receiving simulated acid rain. PLoS One 7:e49664

    CAS  Google Scholar 

  • Zhong H, Liu G, Jiang Y, Yang J, Liu Y, Yang X, Liu Z, Zeng G (2017) Transport of bacteria in porous media and its enhancement by surfactants for bioaugmentation: a review. Biotechnol Adv 35:490–505

    CAS  Google Scholar 

  • Zhu Y, Zhang X, Xie Q, Chen Y, Wang D, Liang Y, Lu J (2005) Solubility and stability of barium arsenateand barium hydrogen arsenate at 25°C. J Hazard Mater 120:37–44. https://doi.org/10.1016/j.jhazmat.2004.12.025

    Article  CAS  Google Scholar 

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Acknowledgements

This study was funded by the Foundation for Research Support of the State of Rio de Janeiro (FAPERJ), the National Council for Scientific and Technological Development (CNPq) and the Coordination for the Improvement of Higher Education Personnel (CAPES). The authors are also grateful to the laboratories of the Technology Center (CT) and the Center of Health Sciences (CCS) of the Federal University of Rio de Janeiro (UFRJ), Brazil. Grant number:141502/2016-9. http://efomento.cnpq.br/efomento/login.do?metodo=apresentar.

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Lopes, C.S.C., Teixeira, D.B., Braz, B.F. et al. Application of rhamnolipid surfactant for remediation of toxic metals of long- and short-term contamination sites. Int. J. Environ. Sci. Technol. 18, 575–588 (2021). https://doi.org/10.1007/s13762-020-02889-5

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