Effect of Bacterial Surfactant along with Application of Chelators on Soluble Cadmium in a Calcareous Soil

Document Type : Research Article

Authors

• S. Arabteymori
• A. Halajnia
• A. Lakzian
• F. Nikbin

Department of Soil Science, Faculty of Agriculture, Ferdowsi University of Mashhad

https://doi.org/10.22067/jsw.2021.71126.1063

Abstract

Introduction
 Surfactants as surface-active substances with combined hydrophobic and hydrophilic properties are widely used in various fields. In soil remediation processes these substances can be used to increase the availability of organic and inorganic contaminants to improve microbial decomposition of organic pollutants or heavy metals adsorption. In recent years, researchers have been seeking to produce and use surfactants that are more environment friendly. In this regard, produced biosurfactants by microorganisms are of special importance due to their environmental benefits. Microorganisms produce a wide range of biosurfactants. Biosurfactants are extracellular compounds that can combine with metals such as zinc, copper, and cadmium and can increase the solubility of these metals and reduce their toxicity. Negatively charged anionic biosurfactants such as rhamnolipids and lipopeptides can increase heavy metals availability by combining to metals and changing the properties of soil solution. In this study, the effect of surfactant application from Pseudomonas putida and Bacillus subtilis and some chelators include sodium citrate, humic acid and Na₂-EDTA on soluble cadmium in a contaminated calcareous soil was investigated.
Materials and Methods
This study was conducted as factorial in a completely randomized design in laboratory conditions at several steps separately. A calcareous soil sample was contaminated with 15 mg kg^-1 cadmium from the source of Cd (NO₃)₂. Contaminated soil incubated for 4 weeks at field capacity. Acid deposition method was used for surfactant extraction from culture medium of Pseudomonas putida KT-2440 and Bacillus subtilis 1795. The structure of extracted biosurfactants was investigated by FTIR. Equilibrium time was obtained by determining the amount of soluble cadmium at times 6, 12, 24, 36, 72 hours by adding 1mM sodium citrate, humic acid and Na₂-EDTA to the contaminated soil (ratio of 1 to 5 soil to solution).
The concentrations of 0, 0.1, 0.25, 0.5, 1 and 2 mM of humic acid, sodium citrate and Na₂-EDTA were used to determine the appropriate concentration of each chelator. To investigate the interaction of chelators and biosurfactants on soluble cadmium, an experimental was conducted as a completely randomized design with factorial arrangement design. Experimental treatments consisted of three types of chelating agents (sodium citrate, humic acid, Na₂-EDTA and control), two types of surfactants from Pseudomonas putida and Bacillus subtilis, and five concentration levels of the biosurfactants (0, 25, 50, 100 mg L^-1).
Results and Discussion
The highest amount of soluble cadmium (11.59 mg L^-1) was observed in Na₂-EDTA treatment at 72 hours, which was significant compared to the other treatments. The lowest amount of soluble cadmium was obtained through application of sodium citrate (0.205 mg L^-1) at 36 hours. In all studied concentrations, Na₂-EDTA had the greatest effect and sodium citrate had the least effect on soluble cadmium. While the use of Na₂-EDTA at all concentrations caused a significant increase in soluble cadmium, sodium citrate had no significant effect on soluble cadmium at studied concentrations. Humic acid at concentrations higher than 0.5 mM significantly increased the soluble cadmium. Increasing the concentration of humic acid and citrate from 1 to 2 mM did not show any significant impact on soluble cadmium. At all levels of biosurfactant application, Na₂-EDTA and humic acid caused a significant increase in soluble cadmium concentration. In control and sodium citrate treatments, application of biosurfactants did not cause significant difference in the concentration of soluble cadmium. The highest amount of soluble cadmium was obtained as a result of the application of Bacillus subtilis surfactant and Na₂-EDTA. However, increasing the concentration of Bacillus subtilis surfactant from 25 to 100 mg L^-1 had no significant effect on increasing the efficiency of Na₂-EDTA.  Pseudomonas putida surfactant had no significant effect on soluble cadmium in Na₂-EDTA application. While in humic acid treatment, the application of the Pseudomonas putida surfactant at the highest concentration (100 mg L^-1) increased the concentration of soluble cadmium. Using Bacillus subtilis surfactant did not have effect on soluble cadmium in application of humic acid.
Conclusion
Among the studied chelators (sodium citrate, humic acid and Na₂-EDTA), Na₂-EDTA had the greatest effect on soluble cadmium. While sodium citrate had no significant effect on soluble cadmium. Surfactants from Pseudomonas putida and Bacillus subtilis had different effects on increasing the efficiency of studied chelators and soluble cadmium in the studied soil. In Na₂-EDTA and humic acid application, surfactant from Bacillus subtilis at a concentration of 25 mg L^-1 and surfactant produced by Pseudomonas putida at a concentration of 100 mg L^-1 had a significant effect on soluble cadmium, respectively. It seems using biosurfactants and chelators on increasing soluble cadmium in soil can be useful for phytoremediation purposes to increase its uptake by plant. However, further research is needed.

Keywords

• Bacillus subtilis
• Bioremediation
• Cadmium
• Pseudomonas putid
• Soil pollution

20.1001.1.20084757.1401.36.1.4.6

Main Subjects

• Soil science

References

1. Babaeian E., Homaee M., and Rahnemaie R. 2016. Chelate-enhanced phytoextraction and phytostabilization of lead-contaminated soils by carrot (Daucus carota). Archives of Agronomy and Soil Science 62: 339-358. https://doi.org/10.1080/03650340.2015.1060320.
2. Baker A.J.M. 2000. Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Phytoremediation of Contaminated Soil and Water. Terry N., and Banuelos G.S. (Eds.). CRC Press. Boca Raton. 85-107.
3. Banat I.M. 1995. Biosurfactants production and use in microbial enhanced oil recovery and pollution remediation: a review. Bioresource Technology 51: 1–12. https://doi.org/10.1016/0960-8524(94)00101-6.
4. Barona A., Aranguiz I., and Elias A. 2001. Metal associations in soils before and after EDTA extractive decontamination: implications for the effectiveness of further cleanup procedures. Environmental Pollution 113: 79–85. https://doi.org/10.1016/S0269-7491(00)00158-5.
5. Berreuter H., Charzinski J., and Scherer S. 2002. Intraspecific diversity of Brevibacterium linens, Corynebacterium glutamicum and Rhodococcus erythropolis based on partial 16S rDNA sequence analysis and Fourier-transform infrared (FT-IR) spectroscopy. Microbiology 148: 1523-1532. https://doi.org/10.1099/00221287-148-5-1523.
6. Broos K., Beyens H., and Smolders E. 2005. Survival of rhizobia in soil is sensitive to elevated zinc in the absence of the host plant. Soil Biology and Biochemistry 37: 573–579. https://doi.org/10.1016/j.soilbio.2004.08.018.
7. Bruna Alice Gomes D.M., Mottal F.L., and Andrade Santana M.H. 2016. Humic acids: Structural properties and multiple functionalities for noveltechnological developments. Materials Science and Engineerinn C 62: 967-974. https://doi.org/10.1016/j.msec.2015.12.001.
8. Chen Y.X., Li Q., Luo Y.M., He Y.F., Zhen, S.J., Yu, Y.L., Tian, G.M., and Wong, M.H. 2003. The role of citric acid on the phytoremediation of heavy metal contaminated soil. Chemosphere 50: 807-811. https://doi.org/10.1016/S0045-6535(02)00223-0.
9. Das P., Mukherjee S., and Sen R. 2008. Antimicrobial potential of a lipopeptide biosurfactant derivedfrom a marine Bacillus circulans. Journal Applied Microbiology 104: 1675-1684. https://doi.org/10.1111/j.1365-2672.2007.03701.x.
10. Etemadian M., Hassani A., Nourzadeh Haddad M., and Hanifei M. 2018. Effect of organic and inorganic acids on the release of nutrients in calcareous soils. Journal of Water and Soil Conservation 24: 73-91. (In Persian with English abstract). 22069/jwsc.2017.12528.2723.
11. Fuguet E., Ràfols C., Rosés M., and Bosch E. 2005. Critical micelle concentration of surfactant in aqueous buffered and unbuffered systems. Analytica Chimica Acta 548: 95-100. https://doi.org/10.1016/j.aca.2005.05.069.
12. Gautam K.K., and Tyagi V.K. 2006. Microbial surfactants: a review. Journal of Oleo Science 55: 155-166. https://doi.org/10.5650/jos.55.155.
13. Gee G.W., and Bauder J.W. 1979. Particle size analysis by hydrometer, a simplified method for routine textural analysis and a sensivity test of measurement parameters. Soil Science Society of America Journal 43: 1004-1007. https://doi.org/10.2136/sssaj1979.03615995004300050038x.
14. Gray C.W., Dunham S.J., Dennis P.G., Zhao F.J. and McGrath S.P. 2006. Fields evaluation of in situ remediation of a heavy metal contaminated soil using lime and red-mud. Environmental Pollution 142: 530-539. https://doi.org/10.1016/j.envpol.2005.10.017.
15. Gunawardana B., Singhal N., and Johnson A. 2011. Effects oF amendments on copper, cadmium and lead phytoextraction by Lolium perenne from multiple-metal contaminated solution. International Journal of Phytoremediation 13: 215–232. https://doi.org/10.1080/15226510903567448.
16. Hofrichter M., and Steinbuchel A. 2001. Biopolymers. Vol. 1: Lignin, humic substances and coal. Wiley Europe-V CH, Weinheim, New York.
17. Hosseini S., Lakzia A., and Halajnia A. 2017. Effect of EDTA and Citric acid on soil enzyme activities and phytoextraction of lead by sun flower and Indian mustard from a contaminated soil. Journal of Water and Soil Conservation 24: 47-65. (In Persian with English abstract). 10.22069/jwfst.2017.12039.2655.
18. Juwarkar A.A., Dubey K.V., Nair A., and Singh S.K. 2008. Bioremediation of multi-metal contaminated soil using biosurfactant-a novel approach. Indian Journal of Microbioogyl 48: 142-146. https://doi.org/10.1007/s12088-008-0014-5.
19. Lagier T., Feuillade G., and Matejka G. 2000. Interactions between copper and organic macromolecules: determination of conditional complexation constants. Agronomie 20: 537-546. https://doi.org/10.1051/agro:2000148.
20. Lambrechts T., Gustot Q., Couder E., Houben D., Iserentant A., and Lutts S. 2011. Comparison of EDTA-enhanced phytoextraction and phytostabilisation strategies with Lolium perenne on a heavy metal contaminated soil. Chemosphere 85: 1290-1298. https://doi.org/10.1016/j.chemosphere.2011.07.034.
21. Lima T.M.S., Procópio L.C., Brandão F.D., Leão B.A., Tótola M.R., and Borges A.C. 2011. Evaluation of bacterial surfactant toxicity towards petroleum degrading microorganisms. Bioresoure Technology 102: 2957-2964. https://doi.org/10.1016/j.biortech.2010.09.109.
22. Loeppert R.H., and Suarez D.L. 1996. Carbonate and Gypsum, Methods of Soil Analysis. Part 3. Chemical Methods. Soil Science Society of America, Madison. https://doi.org/10.2136/sssabookser5.3.c15.
23. Luo C., Shen Z., and Li X. 2005. Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59: 1-11. https://doi.org/10.1016/j.chemosphere.2004.09.100.
24. Makkar R.S., Cameotra S.S., and Banat I.M. Advances in utilization of renewable substrates for biosurfactant production. Applied Microbiology and Biotechnology 1: 1-19. https://doi.org/10.1186/2191-0855-1-5.
25. Muhammad D., Chen F., Zhao G., and Wu F. 2009. Comparison of EDTA and Citric-acid- enhanced phytoextraction of heavy metals in artificially metal contaminated soil by Typha angustifolia. International Journal of Phytoremediation 11: 558-574. https://doi.org/10.1080/15226510902717580.
26. Mulligan C.N., Yong R.N., and Gibbs B.F. 2001. Surfactant-enhanced remediation of contaminated soil: a review. Engineering Geology 60: 371-380. https://doi.org/10.1016/S0013-7952(00)00117-4.
27. Nowack B., Schulin R., and Robinson B.H. 2006. Critical assessment of chelantenhanced metal phytoextraction. Environmental Science & Technology 40: 5225-5232. https://doi.org/10.1021/es0604919.
28. Patowary R., Patowary K., Kalita M.C., and Deka S. 2018. Application of biosurfactant for enhancement of bioremediation process of crude oil contaminated soil. International Biodeterioration and Biodegradation 129: 50-60. https://doi.org/10.1016/j.ibiod.2018.01.004.
29. Phulpoto I.A., Liang H., Yu Z., Hu B., Wang Y., Ndayisenga F., Li J., and Qazi M.A. 2020. Production and characterization of surfactin-like biosurfactant produced by novel strain Bacillus nealsonii S2MT and its potential for oil contaminated soil remediation. Microbial Cell Factories 19: 145-157. https://doi.org/10.1186/s12934-020-01402-4.
30. Pizzeghello D., Francioso O., Ertani A., Muscolo A., and Nardi S. 2013. Isopentenyladenosine and cytokinin-like activity of different humic substances. Journal of Geochemical Exploration 129: 70-75. https://doi.org/10.1016/j.gexplo.2012.10.007.
31. Pornsunthorntawee O., Wongpanit P., Chavadej S., Abe M., and Rujiravanit R. 2008. Structural and physicochemical characterization of crude biosurfactant produced by Pseudomonas aeruginosa SP4 isolated from petroleum-contaminated soil. Bioresource Technology 99: 1589-1595. https://doi.org/10.1016/j.biortech.2007.04.020.
32. Rasouli-Sadaghiani M.H., Karimi H., Ashrafi Saeidlou S., and Khodaverdiloo H. 2019. The Effect of Humic Acid on the Phytoremediation Efficiency of Pb in the Contaminated Soils by Wormwood Plant (Artemicia absantium). Journal of Water and Soil Science (Science and Technology of Agriculture and Natural Resources) 22: 261-278. (in Persian with English abstract). 29252/JSTNAR.22.4.261.
33. Robinson B.H., Brooks R.R., Howes A.W., Kirkman J.H., and Gregg P.E.H. The potential of the high biomass nickel hyper accumulator Berkheya coddii for phytoremediation and phytomining. Journal of Geochemical Exploration 60: 115-126. https://doi.org/10.1016/S0375-6742(97)00036-8.
34. Rong Q., Zhong K., Huang H., Li C., Zhang C., and Nong X. 2020. Humic acid reduces the available cadmium, copper, lead, and zinc in soil and their uptake by Tobacco. Applied Sciences 10: 1-12. https://doi.org/10.3390/app10031077.
35. Rosa C.F.C., Freire D.M.G., and Ferraz E.C. Biosurfactant microfoam: Application in the removal of pollutants from soil. Journal of Environmental Chemical Engineering 3: 89-94. https://doi.org/10.1016/j.jece.2014.12.008.
36. Saichek R.E., and Reddy K.R. 2005. Surfactant-enhanced electrokinetic remediation of polycyclic aromatic hydrocarbons in heterogeneous subsurface environments. Journal of Environmental Engineering and Science 4: 327-339. https://doi.org/10.1139/s04-064.
37. Silva S., Farias C., Rufino R., Luna J., and Arubbo L. 2010. Glycerol as substrate for the production of biosurfactant by Pseudomonas aeruginosa UCP0992. Colloids and Surfaces B: Biointerfaces 79: 174-183. https://doi.org/10.1016/j.colsurfb.2010.03.050.
38. Sun W., Zhu B., Yang F., Dai M., Sehar S., Peng C., Ali I., Naz I. 2021. Optimization of biosurfactant production from Pseudomonas sp. CQ2 and its application for remediation of heavy metal contaminated soil. Chemosphere 265. https://doi.org/10.1016/j.chemosphere.2020.129090.
39. Taheripur A., Kiani Sh., and Hosseinpur A. 2016. Effect of EDTA and citric acid on phytoextraction of copper and zinc from a naturally contaminated soil by maize (Zea mays L.) cultivars. Journal of Water and Soil 29: 1493-1505. (In Persian with English abstract)
40. Tiehm A. 1994. Degradation of polycyclic aromatic hydrocarbons in the presence of synthetic surfactants. Applied Environmental Microbiology 60: 258-263. https://doi.org/10.1128/aem.60.1.258-263.1994
41. Topcuoglu B. 2012. The influence of humic acids on the metal bioavailability and phytoextraction efficiency in longterm sludge applied soil. Conference on International Research on Food Security. Natural Resource Management and Rural Development. Tropentag. Gottingen. Germany.
42. Turgut , Pepe M.K, and Cutright T.J. 2004. The effect of EDTA and citric acid on phytoremediation of Cd, Cr, and Ni from soil using Helianthus annuus. Environmental Pollution 131: 147-154. https://doi.org/10.1016/j.envpol.2004.01.017.
43. Van Hees P.A.W., Jones D.L., and Godbold D.L. 2003. Biodegradation of low molecular weight organic acids in a limed forest soil. Water, Air and Soil Pollution 3: 121-144. https://doi.org/10.1023/A:1024127514103.
44. Volkering F., Breure A.M., and Rulkens W.H. 1998. Microbiological aspects of surfactant use for biological soil remediation. Biodegradation 8: 401-417. https://doi.org/10.1023/A:1008291130109.
45. Walkley A., and Black I.A. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37: 29-38. 1097/00010694-193401000-00003.
46. Wang S., and Mulligan C.N. 2009. Arsenic mobilization from mine tailings in the presence of a biosurfactant. Applied Geochemistry 24: 928-935. https://doi.org/10.1016/j.apgeochem.2009.02.017.
47. Wang Z., Shan X.Q., and Zhang S. 2002. Comparison between fractionation and bioavailability of trace elements in rhizosphere and bulk soils. Chemosphere 46: 1163-1171. https://doi.org/10.1016/S0045-6535(01)00206-5.
48. Wei Z., Wang J.J., Meng Y., Li J., Gaston L.A., Fultz L.M., and DeLaune R.D. 2020. Potential use of biochar and rhamnolipid biosurfactant for remediation of crude oil-contaminated coastal wetland soil: Ecotoxicity assessment, Chemosphere 253: 1-9. https://doi.org/10.1016/j.chemosphere.2020.126617.
49. Wen J., Stacey S.P., McLaughlin M.J., and Kirby J.K .2009. Biodegradation of rhamnolipid, EDTA and citric acid in cadmium and contaminated soils. Soil Biology and Biochemistry 41: 2214-2221. https://doi.org/10.1016/j.soilbio.2009.08.006.
50. Zhang T.H., Wei X.H., Yang B., Xia J.M., Liu C.Y., and Qiu R.L. 2014. Influence of the selective EDTA derivative phenyldiaminetetraacetic acid on the speciation and extraction of heavy metals from a contaminated soil. Chemosphere 109: 1-6. https://doi.org/10.1016/j.chemosphere.2014.02.039.
51. Zhang Y., Yang X., Tian S., Guo W., and Wang J. 2013. The influence of humic acids on the accumulation of lead and cadmium in tobacco leaves grown in different soils. Journal of Soil Science and Plant Nutrition 13: 43-53. http://dx.doi.org/10.4067/S0718-95162013005000005.