The role of bacterial symbionts in the biodegradation of chlorpyrifos in the digestive tract of Plutella xylostella larvae
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Abstract. Hadi MS, Abadi AL, Himawan T, MAsruri, Lestari SR, Rahardjo BT, Aini LQ, Setiawan Y, Tarno H. 2021. The role of bacterial symbionts in the biodegradation of chlorpyrifos in the digestive tract of Plutella xylostella larvae. Biodiversitas 22: 702-712. Several species in the order Lepidoptera act as plant pests, one of which is Plutella xylostella. Plutella xylostella is one of the most destructive pests of cabbage and other horticultural crops. The use of chemical insecticides as pest control for P. xylostella causes many problems, such as the increased pest resistance to pesticides. The objectives of this study are: (i) to obtain and characterize symbiont bacteria in the digestive tract of P. xylostella collected from organic and conventional agriculture soils; (ii) to evaluate the potential of bacterial symbionts in the digestive tract of P. xylostella from organic and conventional soils in degrading the active ingredient of chlorpyrifos insecticide; (iii) To determine the biodegradation process of chlorpyrifos insecticide by symbiont bacteria in the digestive tract of P. xylostella; and (iv) to identify the derivative compounds from the biodegradation of chlorpyrifos insecticide. The results showed 30 symbiont bacteria isolated from the digestive tract of P. xylostella collected from organic soil and 36 symbiont bacteria isolated from the digestive tract of P. xylostella from conventional farming soil. There are 15 species of symbiont bacteria in 5 genera from the digestive tract of P. xylostella from organic and conventional farming capable of degrading the chlorpyrifos insecticide. They are identified as Providencia sp., Pseudomonas sp., Serratia sp., Proteus sp., and Aeromonas sp. Chlorpyrifos-derived compounds from the biodegradation of symbiont bacteria are less toxic than chlorpyrifos compounds.
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References
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Colman D, Toolson E, Takacs-Vesbach C. 2012. Do diet and taxonomy influence insect gut bacteria communities? Mol. Ecol 21: 5124–5137. doi: 10.1111/j.1365-294X.2012.05752.x.
Dellai A, Dridi D, Sakouhi A, Robert J, Djelal J. 2016. Cytotoxic effect of chlorpyrifos ethyl and its degradation derivatives by Pseudomonas peli strain isolated from the Oued Hamdoun River (Tunisia). Toxicol. Ind. Health 32(4): 707–713. doi: 10.1177/0748233713506957.
Duraisamy GS, Mishra AK, Kocábek T, Matoušek J. 2018. Activation of polyketide synthase gene promoter in Cannabis sativa by heterologous transcription factors derived from Humulus lupulus. Biol. Plant 62(2): 250–260. doi: 10.1007/s10535-017-0766-z.
Ebrahimpour B, Yamini Y, Moradi M. 2012. Application of ionic surfactant as a carrier and emulsifier agent for the microextraction of fluoroquinolones. J. Pharm. Biomed. Anal 66: 264–270. doi: https://doi.org/10.1016/j.jpba.2012.03.028.
George N, Chauhan P, Sondhi S, Saini S, Puri N. 2014. Biodegradation and Analytical Methods for Detection of Organophosphorous Pesticide: Chlorpyrifos. Int. J. Pure Appl. Sci. Technol 20: 79–94.
Ghaima K, Rahal NS, Rahal BS, Mohamed MM. 2020. Biodegradation of chlorpyrifos pesticides by xanthomonas bacteria isolated from agricultural soil in baghdad. plant cell Biotechnol. Mol. Biol 21(1–2): 84–90.
Gray MJ, Wholey WY, Jakob U. 2013. Bacterial responses to reactive chlorine species. Annu. Rev. Microbiol 67: 141–160. doi: 10.1146/annurev-micro-102912-142520.
Hernández M, Ojeda M, Martínez–Vázquez J, Villegas-Cornelio, Córdova-Bautista. 2011. OPTIMAL PARAMETERS FOR In Vitro DEVELOPMENT OF THE HYDROCARBONOCLASTIC MICROORGANISM Proteus sp . J. Soil Sci. Plant Nutr 11(9): 29–43.
Ifediegwu M, Awah N, Mbachu A, Okeke C. 2015. Isolation, Growth and Identification of Chlorpyrifos Degrading Bacteria from Agricultural Soil in Anambra State, Nigeria. Univers. J. Microbiol. Res 3: 46–52. doi: 10.13189/ujmr.2015.030402.
Indiragandhi P, Anandham R, Madhaiyan M, Poonguzhali A, Kim GH. 2008. Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos-susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for, antagonism towards entomopathogenic fungi and host insect nutriti. J. Appl. Microbiol 103: 2664–2675. doi: 10.1111/j.1365-2672.2007.03506.x.
Iranzo Rodenas M, Sainz-Pardo, Boluda R, Sánchez J, MORMENEO S. 2001. The use of microorganisms in environmental remediation. Ann. Microbiol. 51.
John E. 2014. Chlorpyrifos Degradation Using Bacterial Consortium Obtained From Soil. Int. J. Environ. Eng. IJEE 1: 91–94.
Kahuthia-Gathu R, Loehr B, Poehling HM. 2008. Development and reproductive potential of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) on cultivated and wild crucifer species in Kenya. Int. J. Trop. Insect Sci. 28: 19–29. doi: 10.1017/S1742758408901375.
Kalshoven LGE. 1981. Pest of Crops In Indonesia. PT. Ichtiar Baru, Jakarta.
Kim JK, Son DW, Kim CH, Cho JH, Marchetti R. 2015. Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope. J. Biol. Chem 290(34): 21042–21053. doi: 10.1074/jbc.M115.651158.
Krieger J. 2010. Single vs. Multiple Sets of Resistance Exercise for Muscle Hypertrophy: A Meta-Analysis. J. Strength Cond. Res 24: 1150–1159. doi: 10.1519/JSC.0b013e3181d4d436.
Li W, Jin D, Shi C, Li F. 2017. Midgut bacteria in deltamethrin-resistant, deltamethrin-susceptible, and field-caught populations of Plutella xylostella, and phenomics of the predominant midgut bacterium Enterococcus mundtii. Sci. Rep. 7. doi: 10.1038/s41598-017-02138-9.
Moekasan TK, Sastrosiswojo S, Rukmana T, Sutanto H, Purnamasri IS. 2004. Status Resistensi Lima Strain Plutella xylostella L. terhadap Formulasi Fipronil, Deltametrin, Profenofos, Abamektin, dan Bacillus thuringiensis. J. Hortik. Vol 14, No 2 Juni 2004. http://ejurnal.litbang.pertanian.go.id/index.php/jhort/article/view/1120.
Paniagua Voirol L, Frago E, Kaltenpoth M, HilkerM, Fatouros N. 2018. Bacterial Symbionts in Lepidoptera: Their Diversity, Transmission, and Impact on the Host. Front. Microbiol 9. doi: 10.3389/fmicb.2018.00556.
Pearson W. 2013. An Introduction to Sequence Similarity (“Homology”) Searching. Curr. Protoc. Bioinformatics Chapter 3: Unit3.1. doi: 10.1002/0471250953.bi0301s42.
Prabaningrum L, Uhan T, Nurwahidah U, Karmin K, Hendra A. 2016. Resistensi Plutella xylostella terhadap Insektisida yang Umum Digunakan oleh Petani Kubis di Sulawesi Selatan. J. Hortik 23: 164. doi: 10.21082/jhort.v23n2.2013.p164-173.
Ramya SL, Venkatesan T, Srinivasa Murthy K, Jalali SK, Verghese A. 2016. Detection of carboxylesterase and esterase activity in culturable gut bacterial flora isolated from diamondback moth, Plutella xylostella (Linnaeus), from India and its possible role in indoxacarb degradation . Brazilian J. Microbiol. 47: 327–336.
Rani M, Lakshmi K, Devi P, Madhuri R, Aruna S. 2008. Isolation and characterization of a chlorpyrifos- degrading bacterium from agricultural soil and its growth response. African J. Microbiol. Res 2: 26–31.
Sarfraz R, Dosdall LM, Keddie B. 2006. Diamondback moth–host plant interactions: Implications for pest management. Crop Prot. - Crop PROT 25: 625–639. doi: 10.1016/j.cropro.2005.09.011.
Sasikala C, Jiwal S, Rout P, Mohandass R. 2012. Biodegradation of chlorpyrifos by bacterial consortium isolated from agriculture soil. World J. Microbiol. Biotechnol 28: 1301–1308. doi: 10.1007/s11274-011-0879-z.
Sastrosiswojo S, Sastrodihardjo S. 1986. Status of biological control of diamondback moth by introduction of parasitoid Diadegma eucerophaga in Indonesia. Lembang, West Java.
Schaad NW, Jones J. 2001. Laboratory Guide for Identification of Plant Pathogenic Bacteria. American Phytopathological Society. St Paul, MN.
Shakeel M, Farooq M, Nasim W, Akram W, Khan FZ. 2017. Environment polluting conventional chemical control compared to an environmentally friendly IPM approach for control of diamondback moth, Plutella xylostella (L.), in China: a review. Environ. Sci. Pollut. Res 24(17): 14537–14550. doi: 10.1007/s11356-017-8996-3.
Shehzadi K, Ahmad M, Bodlah I, Gulzar A. 2015. Susceptibility of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) to some euphorbiaceae plant extracts under laboratory conditions. Asian J. Agric. Biol 2015: 145–149.
Singh B. 2009. Organophosphorus-degrading bacteria: Ecology and industrial applications. Nat. Rev. Microbiol 7: 156–164. doi: 10.1038/nrmicro2050.
Singh B, Walker A, Morgan J, Wright D. 2004. Biodegradation of Chlorpyrifos by Enterobacter Strain B-14 and Its Use in Bioremediation of Contaminated Soils. Appl. Environ. Microbiol 70: 4855–4863. doi: 10.1128/AEM.70.8.4855-4863.2004.
Vischetti C, Casucci C, Perucci P. 2002. Relationship between changes of soil microbial biomass content and imazamox and benfluralin degradation. Biol. Fertil. Soils 35: 13–17. doi: 10.1007/s00374-001-0433-5.
Visôtto LE, Oliveira MGA, Guedes RN, Ribon A, Good PI. 2009. Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. J. Insect Physiol 55: 185–191. doi: 10.1016/j.jinsphys.2008.10.017.
Wilkinson CF. 1976. Insecticide Biochemistry and Physiology (Springer, editor). New York.
Wiyantono, Minarni EW. 2009. Study on Potency Of Liquid Smoke Against The Cabbage Head. J. Pembang. Pedesaan 9(1): 50–56.
Xia X, Zheng D, Zhong H, Qin B, Gurr G. 2013. DNA Sequencing Reveals the Midgut Microbiota of Diamondback Moth, Plutella xylostella (L.) and a Possible Relationship with Insecticide Resistance. PLoS One 8: e68852. doi: 10.1371/journal.pone.0068852.
Xu G, Zheng W, li Y, Wang S, Zhang J. 2008. Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by a newly isolated Paracoccus sp. strain TRP. Int. Biodeterior. Biodegradation 62: 51–56. doi: 10.1016/j.ibiod.2007.12.001.
Zhu J, Zhao YAN, Ruan H. 2019. Comparative study on the biodegradation of chlorpyrifos-methyl by Bacillus megaterium CM-Z19 and Pseudomonas syringae CM-Z6 . An. da Acad. Bras. Ciências 91.
Ardiwinata A, Ginoga L, Sulaeman E, Harsanti E. 2020. Pesticide Residue Monitoring on Agriculture in Indonesia. J. Sumberd. Lahan 12: 133. doi: 10.21082/jsdl.v12n2.2018.133-144.
Colman D, Toolson E, Takacs-Vesbach C. 2012. Do diet and taxonomy influence insect gut bacteria communities? Mol. Ecol 21: 5124–5137. doi: 10.1111/j.1365-294X.2012.05752.x.
Dellai A, Dridi D, Sakouhi A, Robert J, Djelal J. 2016. Cytotoxic effect of chlorpyrifos ethyl and its degradation derivatives by Pseudomonas peli strain isolated from the Oued Hamdoun River (Tunisia). Toxicol. Ind. Health 32(4): 707–713. doi: 10.1177/0748233713506957.
Duraisamy GS, Mishra AK, Kocábek T, Matoušek J. 2018. Activation of polyketide synthase gene promoter in Cannabis sativa by heterologous transcription factors derived from Humulus lupulus. Biol. Plant 62(2): 250–260. doi: 10.1007/s10535-017-0766-z.
Ebrahimpour B, Yamini Y, Moradi M. 2012. Application of ionic surfactant as a carrier and emulsifier agent for the microextraction of fluoroquinolones. J. Pharm. Biomed. Anal 66: 264–270. doi: https://doi.org/10.1016/j.jpba.2012.03.028.
George N, Chauhan P, Sondhi S, Saini S, Puri N. 2014. Biodegradation and Analytical Methods for Detection of Organophosphorous Pesticide: Chlorpyrifos. Int. J. Pure Appl. Sci. Technol 20: 79–94.
Ghaima K, Rahal NS, Rahal BS, Mohamed MM. 2020. Biodegradation of chlorpyrifos pesticides by xanthomonas bacteria isolated from agricultural soil in baghdad. plant cell Biotechnol. Mol. Biol 21(1–2): 84–90.
Gray MJ, Wholey WY, Jakob U. 2013. Bacterial responses to reactive chlorine species. Annu. Rev. Microbiol 67: 141–160. doi: 10.1146/annurev-micro-102912-142520.
Hernández M, Ojeda M, Martínez–Vázquez J, Villegas-Cornelio, Córdova-Bautista. 2011. OPTIMAL PARAMETERS FOR In Vitro DEVELOPMENT OF THE HYDROCARBONOCLASTIC MICROORGANISM Proteus sp . J. Soil Sci. Plant Nutr 11(9): 29–43.
Ifediegwu M, Awah N, Mbachu A, Okeke C. 2015. Isolation, Growth and Identification of Chlorpyrifos Degrading Bacteria from Agricultural Soil in Anambra State, Nigeria. Univers. J. Microbiol. Res 3: 46–52. doi: 10.13189/ujmr.2015.030402.
Indiragandhi P, Anandham R, Madhaiyan M, Poonguzhali A, Kim GH. 2008. Cultivable bacteria associated with larval gut of prothiofos-resistant, prothiofos-susceptible and field-caught populations of diamondback moth, Plutella xylostella and their potential for, antagonism towards entomopathogenic fungi and host insect nutriti. J. Appl. Microbiol 103: 2664–2675. doi: 10.1111/j.1365-2672.2007.03506.x.
Iranzo Rodenas M, Sainz-Pardo, Boluda R, Sánchez J, MORMENEO S. 2001. The use of microorganisms in environmental remediation. Ann. Microbiol. 51.
John E. 2014. Chlorpyrifos Degradation Using Bacterial Consortium Obtained From Soil. Int. J. Environ. Eng. IJEE 1: 91–94.
Kahuthia-Gathu R, Loehr B, Poehling HM. 2008. Development and reproductive potential of diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) on cultivated and wild crucifer species in Kenya. Int. J. Trop. Insect Sci. 28: 19–29. doi: 10.1017/S1742758408901375.
Kalshoven LGE. 1981. Pest of Crops In Indonesia. PT. Ichtiar Baru, Jakarta.
Kim JK, Son DW, Kim CH, Cho JH, Marchetti R. 2015. Insect Gut Symbiont Susceptibility to Host Antimicrobial Peptides Caused by Alteration of the Bacterial Cell Envelope. J. Biol. Chem 290(34): 21042–21053. doi: 10.1074/jbc.M115.651158.
Krieger J. 2010. Single vs. Multiple Sets of Resistance Exercise for Muscle Hypertrophy: A Meta-Analysis. J. Strength Cond. Res 24: 1150–1159. doi: 10.1519/JSC.0b013e3181d4d436.
Li W, Jin D, Shi C, Li F. 2017. Midgut bacteria in deltamethrin-resistant, deltamethrin-susceptible, and field-caught populations of Plutella xylostella, and phenomics of the predominant midgut bacterium Enterococcus mundtii. Sci. Rep. 7. doi: 10.1038/s41598-017-02138-9.
Moekasan TK, Sastrosiswojo S, Rukmana T, Sutanto H, Purnamasri IS. 2004. Status Resistensi Lima Strain Plutella xylostella L. terhadap Formulasi Fipronil, Deltametrin, Profenofos, Abamektin, dan Bacillus thuringiensis. J. Hortik. Vol 14, No 2 Juni 2004. http://ejurnal.litbang.pertanian.go.id/index.php/jhort/article/view/1120.
Paniagua Voirol L, Frago E, Kaltenpoth M, HilkerM, Fatouros N. 2018. Bacterial Symbionts in Lepidoptera: Their Diversity, Transmission, and Impact on the Host. Front. Microbiol 9. doi: 10.3389/fmicb.2018.00556.
Pearson W. 2013. An Introduction to Sequence Similarity (“Homology”) Searching. Curr. Protoc. Bioinformatics Chapter 3: Unit3.1. doi: 10.1002/0471250953.bi0301s42.
Prabaningrum L, Uhan T, Nurwahidah U, Karmin K, Hendra A. 2016. Resistensi Plutella xylostella terhadap Insektisida yang Umum Digunakan oleh Petani Kubis di Sulawesi Selatan. J. Hortik 23: 164. doi: 10.21082/jhort.v23n2.2013.p164-173.
Ramya SL, Venkatesan T, Srinivasa Murthy K, Jalali SK, Verghese A. 2016. Detection of carboxylesterase and esterase activity in culturable gut bacterial flora isolated from diamondback moth, Plutella xylostella (Linnaeus), from India and its possible role in indoxacarb degradation . Brazilian J. Microbiol. 47: 327–336.
Rani M, Lakshmi K, Devi P, Madhuri R, Aruna S. 2008. Isolation and characterization of a chlorpyrifos- degrading bacterium from agricultural soil and its growth response. African J. Microbiol. Res 2: 26–31.
Sarfraz R, Dosdall LM, Keddie B. 2006. Diamondback moth–host plant interactions: Implications for pest management. Crop Prot. - Crop PROT 25: 625–639. doi: 10.1016/j.cropro.2005.09.011.
Sasikala C, Jiwal S, Rout P, Mohandass R. 2012. Biodegradation of chlorpyrifos by bacterial consortium isolated from agriculture soil. World J. Microbiol. Biotechnol 28: 1301–1308. doi: 10.1007/s11274-011-0879-z.
Sastrosiswojo S, Sastrodihardjo S. 1986. Status of biological control of diamondback moth by introduction of parasitoid Diadegma eucerophaga in Indonesia. Lembang, West Java.
Schaad NW, Jones J. 2001. Laboratory Guide for Identification of Plant Pathogenic Bacteria. American Phytopathological Society. St Paul, MN.
Shakeel M, Farooq M, Nasim W, Akram W, Khan FZ. 2017. Environment polluting conventional chemical control compared to an environmentally friendly IPM approach for control of diamondback moth, Plutella xylostella (L.), in China: a review. Environ. Sci. Pollut. Res 24(17): 14537–14550. doi: 10.1007/s11356-017-8996-3.
Shehzadi K, Ahmad M, Bodlah I, Gulzar A. 2015. Susceptibility of diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) to some euphorbiaceae plant extracts under laboratory conditions. Asian J. Agric. Biol 2015: 145–149.
Singh B. 2009. Organophosphorus-degrading bacteria: Ecology and industrial applications. Nat. Rev. Microbiol 7: 156–164. doi: 10.1038/nrmicro2050.
Singh B, Walker A, Morgan J, Wright D. 2004. Biodegradation of Chlorpyrifos by Enterobacter Strain B-14 and Its Use in Bioremediation of Contaminated Soils. Appl. Environ. Microbiol 70: 4855–4863. doi: 10.1128/AEM.70.8.4855-4863.2004.
Vischetti C, Casucci C, Perucci P. 2002. Relationship between changes of soil microbial biomass content and imazamox and benfluralin degradation. Biol. Fertil. Soils 35: 13–17. doi: 10.1007/s00374-001-0433-5.
Visôtto LE, Oliveira MGA, Guedes RN, Ribon A, Good PI. 2009. Contribution of gut bacteria to digestion and development of the velvetbean caterpillar, Anticarsia gemmatalis. J. Insect Physiol 55: 185–191. doi: 10.1016/j.jinsphys.2008.10.017.
Wilkinson CF. 1976. Insecticide Biochemistry and Physiology (Springer, editor). New York.
Wiyantono, Minarni EW. 2009. Study on Potency Of Liquid Smoke Against The Cabbage Head. J. Pembang. Pedesaan 9(1): 50–56.
Xia X, Zheng D, Zhong H, Qin B, Gurr G. 2013. DNA Sequencing Reveals the Midgut Microbiota of Diamondback Moth, Plutella xylostella (L.) and a Possible Relationship with Insecticide Resistance. PLoS One 8: e68852. doi: 10.1371/journal.pone.0068852.
Xu G, Zheng W, li Y, Wang S, Zhang J. 2008. Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by a newly isolated Paracoccus sp. strain TRP. Int. Biodeterior. Biodegradation 62: 51–56. doi: 10.1016/j.ibiod.2007.12.001.
Zhu J, Zhao YAN, Ruan H. 2019. Comparative study on the biodegradation of chlorpyrifos-methyl by Bacillus megaterium CM-Z19 and Pseudomonas syringae CM-Z6 . An. da Acad. Bras. Ciências 91.
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