Skip to main content

Advertisement

SpringerLink
Log in

Effect of chlorpyrifos on the earthworm Eudrilus euginae and their gut microbiome by toxicological and metagenomic analysis

  • Original Paper
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The earthworms are important soil invertebrates and play a crucial role in pedogenesis. The application of pesticides and prolonged exposure to pesticides causes mortality of earthworms apart from profoundly affecting the resident gut microbiome. The microbiome plays a significant effect on the metabolic processes associated with earthworms. The pesticide Chlorpyrifos (CPF) was studied for its toxicity on Eudrilus euginae by toxicity studies. The LC50 value of filter paper contact test and acute toxicity test was 3.8 mg/mL and 180 mg/kg. The prolonged exposure of earthworms to pesticide on reproductive toxicity resulted in the mortality of earthworms and absence of cocoon formation. Further, the effects of CPF on the whole gut microbiome of E. euginae was analyzed using a long amplicon Nanopore sequencing. Results indicated no fluctuations with Firmicutes and Bacteroidetes, that were found to be dominant at bacterial phyla level while at the genus level, remarkable differences were noticed. Clostridium dominated the earthworm gut prior to CPF exposure while Bacillus dominated after exposure. Similarly, the fungal members such as Ascomycota and Basidiomycota were observed to dominate the gut of earthworm at the phyla level before and after exposure to CPF. In contrast, Clavispora (65%) was the dominant genus before CPF exposure and Taloromyces (42%) dominated after the CPF exposure. Our study demonstrates the effect of CPF on the mortality of E. euginae while the amplicon sequencing established the unique microbiome of the gut in response to the CPF exposure.

Graphic abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aamodt S, Konestabo HS, Sverdrup LE, Gudbrandsen M, Reinecke SA, Reinecke AJ, Stenersen J (2007) Recovery of cholinesterase activity in the earthworm Eisenia fetida Savigny following exposure to chlorpyrifos. Environ Toxicol Chem 26(9):1963–1967

    Article  Google Scholar 

  • Alvarenga N, Birolli WG, Seleghim MH, Porto AL (2014) Biodegradation of methyl parathion by whole cells of marine-derived fungi Aspergillus sydowii and Penicillium decaturense. Chemosphere 117:47–52

    Article  Google Scholar 

  • Anwar S, Liaquat F, Khan QM, Khalid ZM, Iqbal S (2009) Biodegradation of chlorpyrifos and its hydrolysis product 3, 5, 6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1. J Hazard Mater 168(1):400–405

    Article  Google Scholar 

  • Baarschers WH, Heitland HS (1986) Biodegradation of fenitrothion and fenitrooxon by the fungus Trichoderma viride. J Agric Food Chem 34(4):707–709

    Article  Google Scholar 

  • Badalato N, Guillot A, Sabarly V, Dubois M, Pourette N, Pontoire B, Robert P, Bridier A, Monnet V, Sousa DZ, Durand S (2017) Whole proteome analyzes on Ruminiclostridiumcellulolyticum show a modulation of the cellulolysis machinery in response to cellulosic materials with subtle differences in chemical and structural properties. PLoS ONE 12(1):e0170524

    Article  Google Scholar 

  • Bhalerao TS, Puranik PR (2007) Biodegradation of organochlorine pesticide, endosulfan, by a fungal soil isolate, Aspergillus niger. Int Biodeterior Biodegrad 59(4):315–321

    Article  Google Scholar 

  • Blakemore RJ (2015) Eco-taxonomic profile of an iconic vermicomposter—the ‘African Nightcrawler’earthworm, Eudrilus eugeniae (Kinberg, 1867). Afr Invertebr 56(3):527–548

    Article  Google Scholar 

  • Booth LH, O’Halloran K (2001) A comparison of biomarker responses in the earthworm Aporrectodea caliginosa to the organophosphorus insecticides diazinon and chlorpyrifos. Environ Toxicol Chem 20(11):2494–2502

    Article  Google Scholar 

  • Boschin G, D’Agostina A, Arnoldi A, Marotta E, Zanardini E, Negri M, Valle A, Sorlini C (2003) Biodegradation of chlorsulfuron and metsulfuron-methyl by Aspergillus niger in laboratory conditions. J Environ Sci Heal B 38(6):737–746

    Article  Google Scholar 

  • Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activityin the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36(3–4):177–198

    Article  Google Scholar 

  • Byzov BA, Khomyakov NV, Kharin SA, Kurakov AV (2007) Fate of soil bacteria and fungi in the gut of earthworms. Eur J Soil Biol 43:S149–S156

    Article  Google Scholar 

  • Byzov BA, Nechitaylo TY, Bumazhkin BK, Kurakov AV, Golyshin PN, Zvyagintsev DG (2009) Culturable microorganisms from the earthworm digestive tract. J Microbiol 78(3):360–368

    Article  Google Scholar 

  • Cai S, Dong X (2010) Cellulosilyticum ruminicola gen. nov., sp. Nov., isolated from the rumen of yak, and reclassification of Clostridium lentocellum as Cellulosilyticum lentocellum comb. Nov. Int J Syst 60(4):845–849

    Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335

    Article  Google Scholar 

  • Carr RL, Ho LL, Chambers JE (1997) Selective toxicity of chlorpyrifos to several species of fish during an environmental exposure: biochemical mechanisms. Environ Toxicol Chem 16(11):2369–2374

    Article  Google Scholar 

  • Chen J, Saleem M, Wang C, Liang W, Zhang Q (2018) Individual and combined effects of herbicide tribenuron-methyl and fungicide tebuconazole on soil earthworm Eisenia fetida. Sci Rep 8(1)

  • Cuscó A, Catozzi C, Viñes J, Sanchez A, Francino O (2018) Microbiota profiling with long amplicons using Nanopore sequencing: full-length 16S rRNA gene and the 16S-ITS-23S of the rrn operon. F1000 Res. https://doi.org/10.12688/f1000research.16817.2

    Article  Google Scholar 

  • Dai YJ, Ji WW, Chen T, Zhang WJ, Liu ZH, Ge F, Yuan S (2010) Metabolism of the neonicotinoid insecticides acetamiprid and thiacloprid by the yeast Rhodotorula mucilaginosa strain IM-2. J Agric Food Chem 58(4):2419–2425

    Article  Google Scholar 

  • Datta S, Singh J, Singh S, Singh J (2016) Earthworms, pesticides and sustainable agriculture: a review. Environ Sci Pollut Res 23(9):8227–8243

    Article  Google Scholar 

  • De Silva PMC, Pathiratne A, van Gestel CA (2010) Toxicity of chlorpyrifos, carbofuran, mancozeb and their formulations to the tropical earthworm Perionyx excavatus. Appl Soil Ecol 44(1):56–60

    Article  Google Scholar 

  • Deb N, Das S (2013) Chlorpyrifos toxicity in fish: a review. Curr World Environ 8(1):77

    Article  Google Scholar 

  • Ding J, Zhu D, Hong B, Wang HT, Li G, Ma YB, Tang YT, Chen QL (2019) Long-term application of organic fertilization causes the accumulation of antibiotic resistome in earthworm gut microbiota. Environ Int 124:145–152

    Article  Google Scholar 

  • Dominguez J, Edwards CA, Dominguez J (2001) The biology and population dynamics of Eudrilus eugeniae (Kinberg) (Oligochaeta) in cattle waste solids. Pedobiologia 45(4):341–353

    Article  Google Scholar 

  • Drake HL, Horn MA (2007) As the worm turns: the earthworm gut as a transient habitat for soil microbial biomes. Annu Rev Microbiol 61:169–189

    Article  Google Scholar 

  • Durrens P, Klopp C, Biteau N, Fitton-Ouhabi V, Dementhon K, Accoceberry I, Sherman DJ, Noël T (2017) Genome sequence of the yeast Clavispora lusitaniae type strain CBS 6936. Genome Announc 5(31):e00724-e817

    Article  Google Scholar 

  • Fernando VK, Perera IC, Dangalle CD, Premawansa S, Wijesinghe MR (2015) Histological alterations in the body wall of the tropical earthworm Eudrilus eugeniae exposed to hexavalent chromium. Bull Environ Contam Toxicol 94(6):744–748

    Article  Google Scholar 

  • Finkelstein ZI, Golovleva LA (1988) Effect of regular application of pesticides on nitrogen bacteria. Z Allg Mikrobiol 143(6):453–456

    Google Scholar 

  • Givaudan N, Wiegand C, Le Bot B, Renault D, Pallois F, Llopis S, Binet F (2014) Acclimation of earthworms to chemicals in anthropogenic landscapes, physiological mechanisms and soil ecological implications. Soil Biol Biochem 73:49–58

    Article  Google Scholar 

  • Gómez-Brandón M, Aira M, Lores M, Domínguez J (2011) Epigeic earthworms exert a bottleneck effect on microbial communities through gut associated processes. PLoS ONE 6(9):e24786

    Article  Google Scholar 

  • Góngora-Echeverría VR, Quintal-Franco C, Arena-Ortiz ML, Giácoman-Vallejos G, Ponce-Caballero C (2018) Identification of microbial species present in a pesticide dissipation process in biobed systems using typical substrates from southeastern Mexico as a biomixture at a laboratory scale. Sci Total Environ 628:528–538

    Article  Google Scholar 

  • Govindarajan B, Prabaharan V (2015) Gut bacterial load analysis of earthworms (Eudrilus eugeniae)–a controlled laboratory study. Eur J Environ Ecol 2:38–43

    Google Scholar 

  • Hammer Ø, Harper DA, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):9

    Google Scholar 

  • Heimbach F (1984) Correlations between three methods for determining the toxicity of chemicals to earthworms. Pestic Sci 15(6):605–611

    Article  Google Scholar 

  • Huang Y, Xiao L, Li F, Xiao M, Lin D, Long X, Wu Z (2018) Microbial degradation of pesticide residues and an emphasis on the degradation of cypermethrin and 3-phenoxy benzoic acid: a review. Molecules 23(9):2313

    Article  Google Scholar 

  • Hundal SS, Kaur R, Kaur A (2016) Effect of chlorpyrifos on survival, growth and reproductive performance of Eudrilus eugeniae (Kinberg). J Nat Appl Sci 8(3):1618–1622

    Article  Google Scholar 

  • Jamieson BGM (1992) Oligochaeta. In: Harrison FW, Gardiner SL (eds) Microscopic anatomy of invertebrates. Wiley, New York, pp 217–322

    Google Scholar 

  • Jeyaprakasam A, Muniyandi B, James AJ, Karmegam N, Ponnuchamy K (2020) Assessment of earthworm diversity and pesticide toxicity in Eudrilus eugeniae. Environ Chem Ecotoxicol 3:23–30

    Article  Google Scholar 

  • John EM, Shaike JM (2015) Chlorpyrifos: pollution and remediation. Environ Chem Lett 13(3):269–291

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Ecosyst Manage. https://doi.org/10.1007/978-1-4612-4018-1_14

    Article  Google Scholar 

  • Kadam DG, Pathade GR (2017) Studies on selected bacteria and glycolytic enzyme activities in the Gut of Eudrilus eugeniae. Int J Curr Microbiol App Sci 6(4):2256–2264

    Article  Google Scholar 

  • Katz EJ, Cortes VI, Eldefrawi ME, Eldefrawi AT (1997) Chlorpyrifos, parathion, and their oxons bind to and desensitize a nicotinic acetylcholine receptor: relevance to their toxicities. Toxicol Appl Pharmacol 146(2):227–236

    Article  Google Scholar 

  • Lakshmi CV, Kumar M, Khanna S (2009) Biodegradation of chlorpyrifos in soil by enriched cultures. Curr Microbiol 58(1):35–38

    Article  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  • Li JW, Fang B, Pang GF, Zhang M, Ren FZ (2019) Age-and diet-specific effects of chronic exposure to chlorpyrifos on hormones, inflammation and gut microbiota in rats. Pestic Biochem Phys 159:68–79

    Article  Google Scholar 

  • Liu YH, Liu Y, Chen ZS, Lian J, Huang X, Chung YC (2004) Purification and characterization of a novel organophosphorus pesticide hydrolase from Penicillium lilacinum BP303. Enzyme Microb Technol 34(3–4):297–303

    Article  Google Scholar 

  • Liu D, Lian B, Wu C, Guo P (2018) A comparative study of gut microbiota profiles of earthworms fed in three different substrates. Symbiosis 74(1):21–29

    Article  Google Scholar 

  • Ma L, Xie Y, Han Z, Giesy JP, Zhang X (2017) Responses of earthworms and microbial communities in their guts to Triclosan. Chemosphere 168:1194–1202

    Article  Google Scholar 

  • Mathur A, Bhat R, Verma SK, Prakash A, Prasad GBKS, Dua VK (2010) Standardization of method for Genomic DNA extraction in Eudrilus eugeniae. Indian J Pharm Sci 9:49–51

    Google Scholar 

  • Meier AB, Hunger S, Drake HL (2018) Differential engagement of fermentative taxa in gut contents of the earthworm Lumbricus terrestris. Appl Environ Microbiol 84(5):e01851-e1917

    Article  Google Scholar 

  • Menon P, Gopal M, Prasad R (2004) Influence of two insecticides, chlorpyrifos and quinalphos, on arginine ammonification and mineralizable nitrogen in two tropical soil types. J Agric Food Chem 52(24):7370–7376

    Article  Google Scholar 

  • Muangphra P, Tharapoom K, Euawong N, Namchote S, Gooneratne R (2016) Chronic toxicity of commercial chlorpyrifos to earthworm Pheretimapeguana. Environ Toxicol 31(11):1450–1459

    Article  Google Scholar 

  • Murugan K, Sindhu R, Umamaheswari S (2010) Eudriluseugeniae-A potent bioremediator in controlling herbicide and pesticide pollution. Int J Pharm 5(5):67–74

    Google Scholar 

  • OECD 207 (1984) Earthworm, Acute toxicity tests. OECD guideline for testing of chemicals

  • Pandey S, Singh DK (2004) Total bacterial and fungal population after chlorpyrifos and quinalphos treatments in groundnut (Arachis hypogaea L.) soil. Chemosphere 55(2):197–205

    Article  Google Scholar 

  • Parthasarathi K, Ranganathan LS, Anandi V, Zeyer J (2007) Diversity of microflora in the gut and casts of tropical composting earthworms reared on different substrates. J Environ Biol 28(1):87–97

    Google Scholar 

  • Pass DA, Morgan AJ, Read DS, Field D, Weightman AJ, Kille P (2015) The effect of anthropogenic arsenic contamination on the earthworm microbiome. Environ Microbiol 17(6):1884–1896

    Article  Google Scholar 

  • Pawar SS, Ahmad S (2014) Filter paper contact test method for estimation of toxic effect of chloropyriphose on earthworm, Eisenia fetida. Int Res J Sci Eng 2(1):23–25

    Google Scholar 

  • Pelosi C, Barot S, Capowiez Y, Hedde M, Vandenbulcke F (2014) Pesticides and earthworms. A review. Agron Sustain Dev 34(1):199–228

    Article  Google Scholar 

  • Rao JV, Pavan YS, Madhavendra SS (2003) Toxic effects of chlorpyrifos on morphology and acetylcholinesterase activity in the earthworm, Eisenia fetida. Ecotoxicol Environ Saf 54(3):296–301

    Article  Google Scholar 

  • Ravindran B, Contreras-Ramos SM, Sekaran G (2015) Changes in earthworm gut associated enzymes and microbial diversity on the treatment of fermented tannery waste using epigeic earthworm Eudrilus eugeniae. Ecol Eng 74:394–401

    Article  Google Scholar 

  • Rayu S, Nielsen UN, Nazaries L, Singh BK (2017) Isolation and molecular characterization of novel chlorpyrifos and 3, 5, 6-trichloro-2-pyridinol-degrading bacteria from sugarcane farm soils. Front Microbiol 8:518

    Article  Google Scholar 

  • Reinecke SA, Reinecke AJ (1999) III. Earthworm ecotoxicology-lysosomal response of earthworm coelomocytes induced by Long-term experimental exposure to heavy metals. Pedobiologia 43(6):585–593

    Google Scholar 

  • Reyes-César A, Absalón ÁE, Fernández FJ, González JM, Cortés-Espinosa DV (2014) Biodegradation of a mixture of PAHs by non-ligninolytic fungal strains isolated from crude oil-contaminated soil. World J Microbiol Biotechnol 30(3):999–1009

    Article  Google Scholar 

  • Rico A, Sabater C, Castillo MÁ (2016) Lethal and sub-lethal effects of five pesticides used in rice farming on the earthworm Eisenia fetida. Ecotoxicol Environ Saf 127:222–229

  • Romero MC, Reinoso EH, Urrutia MI, Moreno Kiernan A (2006) Biosorption of heavy metals by Talaromyces helices: a trained fungus for copper and biphenyl detoxification. Electron J Biotechnol. https://doi.org/10.2225/vol9-issue3-fulltext-11

    Article  Google Scholar 

  • Salam JA, Lakshmi V, Das D, Das N (2013) Biodegradation of lindane using a novel yeast strain, Rhodotorula sp. VITJzN03 isolated from agricultural soil. World J Microbiol Biotechnol 29(3):475–487

    Article  Google Scholar 

  • Sandoval MC, Veiga M, Hinton J, Klein B (2001) Review of biological indicators for metal mining effluents: a proposed protocol using earthworms. In: Proceedings of the 25th annual British Columbia reclamation symposium, 67–79

  • Schulz K, Hunger S, Brown GG, Tsai SM, Cerri CC, Conrad R, Drake HL (2015) Methanogenic food web in the gut contents of methane-emitting earthworm Eudrilus eugeniae from Brazil. ISME J 9(8):1778–1792

    Article  Google Scholar 

  • Shefali G, Gupta RK, Dharambir S (2018) Study to enumerate the alterations in gut bacterial population of Eudrilus eugeniae exposed to sodium arsenate. Int J Curr Microbiol Appl Sci 7(3):596–600

    Article  Google Scholar 

  • Singh A, Singh DP, Tiwari R, Kumar K, Singh RV, Singh S, Prasanna R, Saxena AK, Nain L (2015) Taxonomic and functional annotation of gut bacterial communities of Eisenia fetida and Perionyx excavatus. Microbiol Res 175:48–56

    Article  Google Scholar 

  • Sivakumar S, Anitha P, Ramesh B, Suresh G (2017) Analysis of EAWAG-BBD pathway prediction system for the identification of malathion degrading microbes. Bioinformation 13(3):73

    Article  Google Scholar 

  • Song J, Gu J, Zhai Y, Wu W, Wang H, Ruan Z, Shi Y, Yan Y (2013) Biodegradation of nicosulfuron by a Talaromyces flavus LZM1. Bioresour Technol 140:243–248

    Article  Google Scholar 

  • Šrut M, Menke S, Höckner M, Sommer S (2019) Earthworms and cadmium–heavy metal resistant gut bacteria as indicators for heavy metal pollution in soils? Ecotoxicol Environ Saf 171:843–853

    Article  Google Scholar 

  • Sunaryo T, Widyatmoko H, Rinanti A (2018) Chlorpyrifos removal by Thiobacillus sp. and Clostridium sp. in liquid medium. MATEC Web Conf 197:13012

    Article  Google Scholar 

  • Tamizhazhagan V, Pugazhendy K, Sakthidasan V, Revathi K, Baranitharan M (2016) Investigation of microbial count in the soil and earthworm gut Eudrilus eugeniae. Innov J Agric Sci 4(3):7–9

    Google Scholar 

  • Thakuria D, Schmidt O, Finan D, Egan D, Doohan FM (2010) Gut wall bacteria of earthworms: a natural selection process. ISME J 4(3):357–366

    Article  Google Scholar 

  • Tian Y, Ishikawa H, Yamaguchi T, Yamauchi T, Yokoyama K (2005) Teratogenicity and developmental toxicity of chlorpyrifos: maternal exposure during organogenesis in mice. Reprod Toxicol 20(2):267–270

    Article  Google Scholar 

  • Tiwari RK, Singh S, Pandey RS (2019) Assessment of acute toxicity and biochemical responses to chlorpyrifos, cypermethrin and their combination exposed earthworm, Eudrilus eugeniae. Toxicol Rep 6:288–297

    Article  Google Scholar 

  • Tripathi P, Singh PC, Mishra A, Chauhan PS, Dwivedi S, Bais RT, Tripathi RD (2013) Trichoderma: a potential bioremediator for environmental clean up. Clean Technol Environ Policy 15(4):541–550

    Article  Google Scholar 

  • Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol 46(4):327–338

    Article  Google Scholar 

  • Ukena K, Oumi T, Matsushima O, Ikeda T, Fujita T, Minakata H, Nomoto K (1995) Effects of annetocin, an oxytocin-related peptide isolated from the earthworm Eisenia foetida, and some putative neurotransmitters on gut motility of the earthworm. J Exp Zool 272(3):184–193

    Article  Google Scholar 

  • Vacondio B, Birolli WG, Ferreira IM, Seleghim MH, Gonçalves S, Vasconcellos SP, Porto AL (2015) Biodegradation of pentachlorophenol by marine-derived fungus Trichoderma harzianum CBMAI 1677 isolated from ascidian Didemnun ligulum. Biocatal Agric Biotechnol 4(2):266–275

    Article  Google Scholar 

  • Wacksman MN, Maul JD, Lydy MJ (2006) Impact of atrazine on chlorpyrifos toxicity in four aquatic vertebrates. Arch Environ Contam Toxicol 51(4):681–689

    Article  Google Scholar 

  • Wang HT, Zhu D, Li G, Zheng F, Ding J, O’Connor PJ, Zhu YG, Xue XM (2019) Effects of arsenic on gut microbiota and its biotransformation genes in earthworm Metaphire sieboldi. Environ Sci Technol 53(7):3841–3849

    Article  Google Scholar 

  • White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc 18(1):315–322

    Google Scholar 

  • Wüst PK, Horn MA, Drake HL (2011) Clostridiaceae and Enterobacteriaceae as active fermenters in earthworm gut content. ISME J 5(1):92–106

    Article  Google Scholar 

  • Yasmin S, D'Souza D (2010) Effects of pesticides on the growth and reproduction of earthworm: a review. Appl Environ Soil Sci 2010:1–9

    Article  Google Scholar 

  • Zhang S, Yin L, Liu Y, Zhang D, Luo X, Cheng JE, Cheng F, Dai J (2011) Cometabolic biotransformation of fenpropathrin by Clostridium species strain ZP3. Biodegradation 22(5):869–875

    Article  Google Scholar 

  • Zhao RB, Bao HY, Liu YX (2010) Isolation and characterization of Penicillium oxalicum ZHJ6 for biodegradation of methamidophos. Agric Sci China 9(5):695–703

    Article  Google Scholar 

  • Zhu J, Zhao Y, Ruan H (2019) Comparative study on the biodegradation of chlorpyrifos-methyl by Bacillus megaterium CM-Z19 and Pseudomonas syringae CM-Z6. An Acad Bras Ciênc. https://doi.org/10.1590/0001-3765201920180694

    Article  Google Scholar 

Download references

Acknowledgement

We would like to thank DBT FOLDSCOPE (2018–2019)—BT/IN/Indo-US/Foldscope/39/2015 for funding this project. We would also like to extend our gratitude to the Management, Stella Maris College (Autonomous), Chennai.

Author information

Author notes

  1. Shruthi Ganesh and Suryasri Kalidas have contributed equally.

Authors and Affiliations

  1. Department of Biotechnology, Stella Maris College (Autonomous), Affiliated to University of Madras, Chennai, India

    Veena Gayathri Krishnaswamy, Mariyam Fathima Jaffar & Rajalakshmi Sridharan

  2. Center for Molecular Medicine and Therapeutics, PSG Institute of Medical Sciences and Research, Coimbatore, India

    Shruthi Ganesh, Suryasri Kalidas & Kabilan Mani

  3. Department of Biotechnology, PSG College of Technology, Coimbatore, India

    Vignesh Palanisamy

Authors
  1. Veena Gayathri Krishnaswamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mariyam Fathima Jaffar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rajalakshmi Sridharan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shruthi Ganesh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Suryasri Kalidas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vignesh Palanisamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kabilan Mani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Veena Gayathri Krishnaswamy or Kabilan Mani.

Ethics declarations

Ethical approval

The Reference number of the ethical committee report is SMC/REC/2021/001.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2486 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krishnaswamy, V.G., Jaffar, M.F., Sridharan, R. et al. Effect of chlorpyrifos on the earthworm Eudrilus euginae and their gut microbiome by toxicological and metagenomic analysis. World J Microbiol Biotechnol 37, 76 (2021). https://doi.org/10.1007/s11274-021-03040-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-021-03040-3

Keywords

Search

Navigation