DOI QR코드

DOI QR Code

Evaluation of the Synergistic Effect of Mixed Cultures of White-Rot Fungus Pleurotus ostreatus and Biosurfactant-Producing Bacteria on DDT Biodegradation

  • Purnomo, Adi Setyo (Department of Chemistry, Faculty of Mathematics and Natural Sciences, Institut Teknologi Sepuluh Nopember (ITS), Kampus ITS Sukolilo) ;
  • Ashari, Khoirul (Department of Chemistry, Faculty of Mathematics and Natural Sciences, Institut Teknologi Sepuluh Nopember (ITS), Kampus ITS Sukolilo) ;
  • Hermansyah, Farizha Triyogi (Department of Chemistry, Faculty of Mathematics and Natural Sciences, Institut Teknologi Sepuluh Nopember (ITS), Kampus ITS Sukolilo)
  • Received : 2017.01.31
  • Accepted : 2017.04.20
  • Published : 2017.07.28

Abstract

DDT (1,1,1-trichloro-2,2-bis(4-chlorophenyl) ethane) is one of the organic synthetic pesticides that has many negative effects for human health and the environment. The purpose of this study was to investigate the synergistic effect of mixed cutures of white-rot fungus, Pleurotus ostreatus, and biosurfactant-producing bacteria, Pseudomonas aeruginosa and Bacillus subtilis, on DDT biodegradation. Bacteria were added into the P. ostreatus culture (mycelial wet weight on average by 8.53 g) in concentrations of 1, 3, 5, and 10 ml ($1ml{\approx}1.25{\times}10^9$ bacteria cells/ml culture). DDT was degraded to approximately 19% by P. ostreatus during the 7-day incubation period. The principal result of this study was that the addition of 3 ml of P. aeruginosa into P. ostreatus culture gave the highest DDT degradation rate (approximately 86%) during the 7-day incubation period. This mixed culture combination of the fungus and bacteria also gave the best ratio of optimization of 1.91. DDD (1,1-dichloro-2,2-bis(4-chlorophenyl) ethane), DDE (1,1-dichloro-2,2-bis(4-chlorophenyl) ethylene), and DDMU (1-chloro-2,2-bis(4-chlorophenyl) ethylene) were detected as metabolic products from the DDT degradation by P. ostreatus and P. aeruginosa. The results of this study indicate that P. aeruginosa has a synergistic relationship with P. ostreatus and can be used to optimize the degradation of DDT by P. ostreatus.

Keywords

References

  1. Boul HL. 1995. DDT residues in the environment - a review with a New Zealand perspective. N.Z. J. Agric. Res. 38: 257-277. https://doi.org/10.1080/00288233.1995.9513126
  2. Busvine JR. 1989. DDT: fifty years for good or ill. Pestic. Outlook 1: 4-8.
  3. Foght J, April T, Biggar K, Aislabie J. 2001. Bioremediation of DDT-contaminated soils: a review. Bioremediat. J. 5: 225-246. https://doi.org/10.1080/20018891079302
  4. Kale SP, Murthy NBK, Raghu K, Sherkhane PD, Carvalho FP. 1999. Studies on degradation of $^{14}C$-DDT in the marine environment. Chemosphere 39: 959-968. https://doi.org/10.1016/S0045-6535(99)00027-2
  5. Aislabie JM, Richards NK, Boul HL. 1997. Microbial degradation of DDT and its residues - a review. N.Z. J. Agric. Res. 40: 269-282. https://doi.org/10.1080/00288233.1997.9513247
  6. Simonich SL, Hites RA. 1995. Global distribution of persistent organochlorine compounds. Science 269: 1851-1854. https://doi.org/10.1126/science.7569923
  7. Purnomo AS, Kamei I, Kondo R. 2008. Degradation of 1,1,1- trichloro-2,2-bis (4-chlorophenyl) ethane (DDT) by brown-rot fungi. J. Biosci. Bioeng. 105: 614-621. https://doi.org/10.1263/jbb.105.614
  8. Purnomo AS, Mori T, Kamei I, Nishii T, Kondo R. 2010. Application of mushroom waste medium from Pleurotus ostreatus for bioremediation of DDT-contaminated soil. Int. Biodeterior. Biodegrad. 64: 397-402. https://doi.org/10.1016/j.ibiod.2010.04.007
  9. Abalos A, Pinazo A, Infante MR, Casals M, Garcia F, Manresa A. 2001. Physicochemical and antimicrobial properties of new rhamnolipids produced by Pseudomonas aeruginosa AT10 from soybean oil refinery wastes. Langmuir 17: 1367-1371. https://doi.org/10.1021/la0011735
  10. Datta S. 2011. Optimization of culture conditions for biosurfactant production from Pseudomonas aeruginosa OCD1. J. Adv. Sci. Res. 2: 32-36.
  11. Guerra-Santos L, Kappeli O, Fiechter A. 1984. Pseudomonas aeruginosa biosurfactant production in continuous culture with glucose as carbon source. Appl. Environ. Microbiol. 48: 301-305.
  12. Rahman KSM, Rahman TJ, McClean S, Marchant R, Banat IM. 2002. Rhamnolipid biosurfactant production by strains of Pseudomonas aeruginosa using low-cost raw materials. Biotechnol. Prog. 18: 1277-1281. https://doi.org/10.1021/bp020071x
  13. 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 Biointerfaces 79: 174-183. https://doi.org/10.1016/j.colsurfb.2010.03.050
  14. Yin H, Qiang J, Jia Y, Ye J, Peng H, Qin H, et al. 2009. Characteristics of biosurfactant produced by Pseudomonas aeruginosa S6 isolated from oil-containing wastewater. Process Biochem. 44: 302-308. https://doi.org/10.1016/j.procbio.2008.11.003
  15. Zhang C, Wang S, Yan Y. 2012. Isomerization and biodegradation of beta-cypermethrin by Pseudomonas aeruginosa CH7 with biosurfactant production. Bioresour. Technol. 102: 7139-7146.
  16. Gudina EJ, Rangarajan V, Sen R, Rodrigues LR. 2013. Potential therapeutic applications of biosurfactants. Trends Pharmacol. Sci. 34: 667-675. https://doi.org/10.1016/j.tips.2013.10.002
  17. Pornsunthorntawee N, Arttaweeporn N, Paisanjit S, Somboonthanate P, Abe M, Rujiravanit R, et al. 2008. Isolation and comparison of biosurfactants produced by Bacillus subtilis Pt2 and Pseudomonas aeruginosa SP4 for microbial surfactant-enhanced oil recovery. Biochem. Eng. J. 42: 172-179. https://doi.org/10.1016/j.bej.2008.06.016
  18. Zouari R, Chaabouni SE, Aydi DG. 2014. Optimization of Bacillus subtilis SPB1 biosurfactant production under solidstate fermentation using by-products of a traditional olive mill factory. Achiev. Life Sci. 8: 162-169. https://doi.org/10.1016/j.als.2015.04.007
  19. Bidlan R. 2003. Studies on DDT degradation by bacterial strains. PhD Thesis, Central Food Technological Research Institute, University of Mysore, India.
  20. Golovleva L, Skryabin GK. 1980. Degradation of DDT and its analogs by Pseudomonas aeruginosa 640x. Biol. Bull. Acad. Sci. USSR 7: 143-151.
  21. Bumpus JA. 1995. Microbial degradation of azo dyes, pp. 157-175. In Singh VP (ed.), Biotransformations: Microbial Degradation of Health-Risk Compounds. Elsevier Science, Amsterdam. The Netherlands.
  22. Cho EA, Seo J, Lee DW, Pan JG. 2011. Decolorization of indigo carmine by laccase displayed on Bacillus subtilis spores. Enzyme Microb. Technol. 49: 100-104. https://doi.org/10.1016/j.enzmictec.2011.03.005
  23. Farzaneh M, Shi ZQ, Ghassempour A, Sedaghat N, Ahmadzadeh M, Mirabolfathy M, et al. 2012. Aflatoxin B1 degradation by Bacillus subtilis UTBSP1 isolated from pistachio nuts of Iran. Food Control 23: 100-106. https://doi.org/10.1016/j.foodcont.2011.06.018
  24. Sompornpailin D, Siripattanakul-Ratpukdi S, Vangnai AS. 2014. Diethyl phthalate degradation by the freeze-dried, entrapped Bacillus subtilis strain 3C3. Int. Biodeterior. Biodegrad. 91: 138-147. https://doi.org/10.1016/j.ibiod.2014.02.004
  25. Johnson BT, Kennedy JO. 1973. Biomagnification of p,p'- DDT and methoxychlor by bacteria. Appl. Microbiol. 26: 66-71.
  26. Langlois BE, Collins JA, Sides KG. 1970. Some factors affecting degradation of organochlorine pesticide by bacteria. J. Dairy Sci. 53: 1671-1675. https://doi.org/10.3168/jds.S0022-0302(70)86461-X
  27. Purnomo AS, Mori T, Kondo R. 2010. Involvement of Fenton reaction in DDT degradation by brown-rot fungi. Int. Biodeterior. Biodegrad. 64: 560-565. https://doi.org/10.1016/j.ibiod.2010.06.008
  28. Purnomo AS, Mori T, Putra SR, Kondo R. 2013. Biotransformation of heptachlor and heptachlor epoxide by white-rot fungus Pleurotus ostreatus. Int. Biodeterior. Biodegrad. 82: 40-44. https://doi.org/10.1016/j.ibiod.2013.02.013
  29. Purnomo AS, Nawfa R, Martak F, Shimizu K, Kamei I. 2017. Biodegradation of aldrin and dieldrin by white-rot fungus Pleurotus ostreatus. Curr. Microbiol. 74: 320-324. https://doi.org/10.1007/s00284-016-1184-8
  30. Wahyuni S, Suhartono MT, Khaeruni A, Purnomo AS, Asranudin, Holilah, Riupassa PA. 2016. Purification and characterization of thermostable chitinase from Bacillus SW41 for chitin oligomer production. Asian J. Chem. 28: 2731-2736. https://doi.org/10.14233/ajchem.2016.20099
  31. Purnomo AS, Mori T, Takagi K, Kondo R. 2011. Bioremediation of DDT contaminated soil using brown-rot fungi. Int. Biodeterior. Biodegrad. 65: 691-695. https://doi.org/10.1016/j.ibiod.2011.04.004
  32. Purnomo AS, Koyama F, Mori T, Kondo R. 2010. DDT degradation potential of cattle manure compost. Chemosphere 80: 619-624. https://doi.org/10.1016/j.chemosphere.2010.04.059
  33. Purnomo AS, Mori T, Kamei I, Kondo R. 2011. Basic studies and applications on bioremediation of DDT: a review. Int. Biodeterior. Biodegrad. 65: 921-930. https://doi.org/10.1016/j.ibiod.2011.07.011
  34. Purnomo AS, Putra SR, Shimizu K, Kondo R. 2014. Biodegradation of heptachlor and heptachlor epoxidecontaminated soils by white-rot fungal inocula. Environ. Sci. Pollut. Res. 21: 11305-11312. https://doi.org/10.1007/s11356-014-3026-1
  35. Subba Rao RV, Alexander M. 1985. Bacterial and fungal cometabolism of 1,1,1-trichloro-2,2-bis-(4-chlorophenyl) ethane (DDT) and its breakdown products. Appl. Environ. Microbiol. 49: 509-516.
  36. Arisoy M. 1998. Biodegradation of chlorinated organic compounds by white-rot fungi. Bull. Environ. Contam. Toxicol. 60: 872-876. https://doi.org/10.1007/s001289900708
  37. Bumpus JA, Aust SD. 1987. Biodegradation of DDT [1,1,1- tri-chloro-2,2-bis(4-chlorophenyl) ethane] by the white rot fungus Phanerochaete chrysosporium. Appl. Environ. Microbiol. 53: 2001-2008.
  38. Shah MM, Barr DP, Chang N, Aust SD. 1992. Use of white rot fungi in the degradation of environmental chemicals. Toxicol. Lett. 64/65: 493-501. https://doi.org/10.1016/0378-4274(92)90224-8
  39. Xiao P, Mori T, Kamei I, Kondo R. 2011. A novel metabolic pathway for biodegradation of DDT by white rot fungi, Phlebia lindtneri and Phlebia brevispora. Biodegradation 22: 859-867. https://doi.org/10.1007/s10532-010-9443-z
  40. Wedemeyer G. 1966. Dechlorination of DDT by Aerobacter aerogenes. Science 152: 647.
  41. Wedemeyer G. 1967. Dechlorination of 1,1,1-trichloro-2,2- bis(p-chlorophenyl) ethane by Aerobacter aerogenes. Appl. Microbiol. 15: 569-574.
  42. Patil KC, Matsumura F, Boush GM. 1970. Degradation of endrin, aldrin, and DDT by soil microorganisms. Appl. Environ. Microbiol. 19: 879-881.
  43. Pfaender FK, Alexander M. 1972. Extensive microbial degradation of DDT in vitro and DDT metabolism by natural communities. J. Agric. Food Chem. 20: 842-846. https://doi.org/10.1021/jf60182a045
  44. Focht DD, Alexander M. 1970. DDT metabolites and analogs: ring fission by Hydrogenomonas. Science 170: 91-92. https://doi.org/10.1126/science.170.3953.91
  45. Focht DD, Alexander M. 1971. Aerobic cometabolism of DDT analogues by Hydrogenomonas sp. J. Agric. Food Chem. 19: 20-22. https://doi.org/10.1021/jf60173a042
  46. Nadeau LJ, Mann FM, Breen A, Sayler GS. 1994. Aerobic degradation of 1,1,1-trichloro-2,2-bis-(4-chlorophenyl) ethane (DDT) by Alcaligenes eutrophus A5. Appl. Environ. Microbiol. 60: 51-55.
  47. Pesce SF, Wunderlin DA. 2004. Biodegradation of lindane by a native bacterial consortium isolated from contaminated river sediment. Int. Biodeterior. Biodegrad. 54: 255-260. https://doi.org/10.1016/j.ibiod.2004.02.003
  48. Kamanavalli CM, Ninnekar HZ. 2004. Biodegradation of DDT by a Pseudomonas species. Curr. Microbiol. 48: 10-13. https://doi.org/10.1007/s00284-003-4053-1
  49. Fang H, Dong B, Yan H, Tang F, Yu Y. 2010. Characterization of a bacterial strain capable of degrading DDT congeners and its use in bioremediation of contaminated soil. J. Hazard. Mater. 184: 281-289. https://doi.org/10.1016/j.jhazmat.2010.08.034
  50. Kantachote D, Singleton I, McClure N, Naidu R, Megharaj M, Harch BD. 2003. DDT resistance and transformation by different microbial strains isolated from DDT-contaminated soils and compost materials. Compost Sci. Util. 11: 300-310. https://doi.org/10.1080/1065657X.2003.10702139
  51. Bajaj A, Mayilraj S, Mudiam MK, Patel DK, Manickam N. 2014. Isolation and functional analysis of a glycolipid producing Rhodococcus sp. strain IITR03 with potential for degradation of 1,1,1-trichloro-2,2-bis(4-chlorophenyl) ethane (DDT). Bioresour. Technol. 167: 398-406. https://doi.org/10.1016/j.biortech.2014.06.007
  52. Wang S, Nomura N, Nakajima T, Uchiyama H. 2012. Case study of the relationship between fungi and bacteria associated with high-molecular-weight polycyclic aromatic hydrocarbon degradation. J. Biosci. Bioeng. 113: 624-630. https://doi.org/10.1016/j.jbiosc.2012.01.005
  53. Hai FI, Modin O, Yamamoto K, Fukushi K, Nakajima F. 2012. Pesticide removal by a mixed culture of bacteria and white-rot fungi. J. Taiwan Inst. Chem. Eng. 43: 459-462. https://doi.org/10.1016/j.jtice.2011.11.002
  54. Ge S, Liu L, Xue Q, Yuan Z. 2016. Effects of exogenous aerobic bacteria on methane production and biodegradation of municipal solid waste in bioreactors. Waste Manag. 55: 93-98. https://doi.org/10.1016/j.wasman.2015.11.024
  55. Mata-Sandoval JC, Karns J, Torrents A. 2001. Influence of rhamnolipids and Triton X-100 on the biodegradation of three pesticides in aqueous and soil slurries. J. Agric. Food Chem. 49: 3296-3303. https://doi.org/10.1021/jf001432w
  56. Deepika KV, Kalam S, Sridhar PR, Podile AR, Bramhachari PV. 2016. Optimization of rhamnolipid biosurfactant production by mangrove sediment bacterium Pseudomonas aeruginosa KVD-HR42 using response surface methodology. Biocatal. Agric. Biotechnol. 5: 38-47.
  57. El-Sheshtawy HS, Doheim MM. 2014. Selection of Pseudomonas aeruginosa for biosurfactant production and studies of its antimicrobial activity. Egypt. J. Petrol. 23: 1-6. https://doi.org/10.1016/j.ejpe.2014.02.001
  58. 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
  59. Wang T, Liang Y, Wu M, Chen Z, Lin J, Yang L. 2015. Natural products from Bacillus subtilis with antimicrobial properties. Chinese J. Chem. Eng. 23: 744-754. https://doi.org/10.1016/j.cjche.2014.05.020
  60. Zheng G , Selvam A , Wong JW. 2012. Oil-in-water microemulsions enhance the biodegradation of DDT by Phanerochaete chrysosporium. Bioresour. Technol. 126: 397-403. https://doi.org/10.1016/j.biortech.2012.02.141
  61. Betancur-Corredor B, Pino NJ, Cardona S, Penuela GA. 2015. Evaluation of biostimulation and Tween 80 addition for the bioremediation of long-term DDT-contaminated soil. J. Environ. Sci. 28: 101-109. https://doi.org/10.1016/j.jes.2014.06.044
  62. Buswell JA, Cai Y J, Chang ST. 1993. Fungal- and substrateassociated factors affecting the ability of individual mushroom species to utilize different lignocellulosic growth substrates, pp. 141-150. In Chang S, Buswell JA, Chiu S (eds.), Mushroom Biology and Mushroom Products. The Chinese University Press, Hong Kong.
  63. Masaphy S, Levanon D, Henis Y, Venkateswrlu K, Kelly SL. 1995. Microsomal and cytosolic cytochrome-P450 mediated benzo(a)pyrene hydroxylation in Pleurotus pulmonarius. Biotechnol. Lett. 17: 969-974. https://doi.org/10.1007/BF00127436
  64. Masaphy S, Levanon D, Henis Y, Venkateswarlu K, Kelly SL. 1996. Evidence for cytochrome P-450 and P-450-mediated benzo(a)pyrene hydroxylation in the white rot fungus Phanerochaete chrysosporium. FEMS Microbiol. Lett. 135: 51-55. https://doi.org/10.1111/j.1574-6968.1996.tb07965.x
  65. Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia CE. 1996. Initial oxidation products in the metabolism of pyrene, anthracene, fluorene, and dibenzothiophene by the white rot fungus Pleurotus ostreatus. Appl. Environ. Microbiol. 62: 2554-2559.
  66. Kamei I, Kondo R. 2005. Biotransformation of dichloro-, trichloro-, and tetrachlorodibenzo-p-dioxin by the white-rot fungus Phlebia lindtneri. Appl. Microbiol. Biotechnol. 68: 560-566. https://doi.org/10.1007/s00253-005-1947-9
  67. Kamei I, Sonoki S, Haraguchi K, Kondo R. 2006. Fungal bioconversion of toxic polychlorinated biphenyls by white-rot fungus, Phlebia brevispora. Appl. Microbiol. Biotechnol. 73: 932-940. https://doi.org/10.1007/s00253-006-0529-9
  68. Mori T, Kondo R. 2002. Oxidation of chlorinated dibenzo-pdioxin and dibenzofuran by white-rot fungus, Phlebia lindtneri. FEMS Microbiol. Lett. 216: 223-227. https://doi.org/10.1111/j.1574-6968.2002.tb11439.x
  69. Mori T, Nakamura K, Kondo R. 2009. Fungal hydroxylation of polychlorinated naphthalenes with chlorine migration by wood rotting fungi. Chemosphere 77: 1230-1235. https://doi.org/10.1016/j.chemosphere.2009.08.046
  70. Hiratsuka N, Wariishi H, Tanaka H. 2001. Degradation of diphenyl ether herbicides by the lignin-degrading basidiomycete Coriolus versicolor. Appl. Microbiol. Biotechnol. 57: 563-571. https://doi.org/10.1007/s002530100789
  71. Cuany A, Pralavorio M, Pauron D, Berge JB, Fournier D, Blais C. 1990. Characterization of microsomal oxidative activities in a wild-type and in a DDT resistant strain of Drosophila melanogaster. Pestic. Biochem. Physiol. 37: 293-302. https://doi.org/10.1016/0048-3575(90)90136-P
  72. Joussen N, Heckel DG, Haas M, Schuphan I, Schmidt B. 2008. Metabolism of imidacloprid and DDT by P450 CYP6G1 expressed in cell cultures of Nicotiana tabacum suggests detoxification of these insecticides in Cyp6g1-overexpressing strains of Drosophila melanogaster, leading to resistance. Pest Manag. Sci. 64: 65-73. https://doi.org/10.1002/ps.1472
  73. Suhara H, Adachi A, Kamei I, Maekawa N. 2011. Degradation of chlorinated pesticide DDT by litter-decomposing basidiomycetes. Biodegradation 22: 1075-1086. https://doi.org/10.1007/s10532-011-9464-2
  74. Bidlan M, Manonmani HK. 2002. Aerobic degradation of dichlorodiphenyltrichloroethane (DDT) by Serratia marcescens DT-1P. Process Biochem. 38: 49-56. https://doi.org/10.1016/S0032-9592(02)00066-3
  75. Li FB, Li XM, Zhou SG, Zhuang L, Cao F, Huang DY, et al. 2010. Enhanced reductive dechlorination of DDT in an anaerobic system of dissimilatory iron-reducing bacteria and iron oxide. Environ. Pollut. 158: 1733-1740. https://doi.org/10.1016/j.envpol.2009.11.020
  76. Bao P, Hu ZY, Wang XJ, Chen J, Ba YX, Hua J, et al. 2012. Dechlorination of p,p'-DDTs coupled with sulfate reduction by novel sulfate-reducing bacterium Clostridium sp BXM. Environ. Pollut. 162: 303-310. https://doi.org/10.1016/j.envpol.2011.11.037

Cited by

  1. Abilities of Co-Cultures of White-Rot Fungus Ganoderma lingzhi and Bacteria Bacillus subtilis on Biodegradation DDT vol.1095, pp.None, 2017, https://doi.org/10.1088/1742-6596/1095/1/012015
  2. A Novel Action of Endocrine-Disrupting Chemicals on Wildlife; DDT and Its Derivatives Have Remained in the Environment vol.19, pp.5, 2017, https://doi.org/10.3390/ijms19051377
  3. Bio-decolorization and novel bio-transformation of methyl orange by brown-rot fungi vol.16, pp.11, 2017, https://doi.org/10.1007/s13762-019-02484-3
  4. Bio-removal of tetracycline antibiotics under the consortium with probiotics Bacillus clausii T and Bacillus amyloliquefaciens producing biosurfactants vol.710, pp.None, 2017, https://doi.org/10.1016/j.scitotenv.2019.136329
  5. Biofilms Provide New Insight into Pesticide Occurrence in Streams and Links to Aquatic Ecological Communities vol.54, pp.9, 2017, https://doi.org/10.1021/acs.est.9b07430
  6. Synergistic interaction of a consortium of the brown-rot fungus Fomitopsis pinicola and the bacterium Ralstonia pickettii for DDT biodegradation vol.6, pp.6, 2017, https://doi.org/10.1016/j.heliyon.2020.e04027
  7. An innovative co-fungal treatment to poplar bark sawdust for delignification and polyphenol enrichment vol.157, pp.None, 2017, https://doi.org/10.1016/j.indcrop.2020.112896
  8. Tapping the Role of Microbial Biosurfactants in Pesticide Remediation: An Eco-Friendly Approach for Environmental Sustainability vol.12, pp.None, 2017, https://doi.org/10.3389/fmicb.2021.791723