Skip to main content

Advertisement

SpringerLink
Log in

Biodegradation of the neonicotinoid insecticide thiamethoxam by the nitrogen-fixing and plant-growth-promoting rhizobacterium Ensifer adhaerens strain TMX-23

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Thiamethoxam (THIA), a second generation neonicotinoid insecticide in the thianicotinyl subclass, is used worldwide. Environmental studies revealed that microbial degradation is the major mode of removal of this pesticide from soil. However, microbial transformation of THIA is poorly understood. In the present study, we isolated a bacterium able to degrade THIA from rhizosphere soil. The bacterium was identified as Ensifer adhaerens by its morphology and 16S ribosomal DNA sequence analysis. High-performance liquid chromatography and mass spectrometry analysis suggested that the major metabolic pathway of THIA in E. adhaerens TMX-23 involves the transformation of its N-nitroimino group (=N–NO2) to N-nitrosoimino (=N–NO) and urea (=O) metabolites. E. adhaerens TMX-23 is a nitrogen-fixing bacterium harboring two types of nifH genes in its genome, one of which is 98 % identical to the nifH gene in the cyanobacterium Calothrix sp. MCC-3A. E. adhaerens TMX-23 released various plant-growth-promoting substances including indole-3-acetic acid, exopolysaccharides, ammonia, HCN, and siderophores. Inoculation of E. adhaerens TMX-23 onto soybean seeds (Glycine max L.) with NaCl at 50, 100, or 154 mmol/L increased the seed germination rate by 14, 21, and 30 %, respectively. THIA at 10 mg/L had beneficial effects on E. adhaerens TMX-23, enhancing growth of the bacterium and its production of salicylic acid, an important plant phytohormone associated with plant defense responses against abiotic stress. The nitrogen-fixing and plant-growth-promoting rhizobacterium E. adhaerens TMX-23, which is able to degrade THIA, has the potential for bioaugmentation as well as to promote growth of field crops in THIA-contaminated soil.

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

  • Ahemad M, Khan MS (2011a) Effects of insecticides on plant-growth-promoting activities of phosphate solubilizing rhizobacterium Klebsiella sp. strain PS19. Pestic Biochem Phys 100:51–56

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2011b) Ecotoxicological assessment of pesticides towards the plant growth promoting activities of Lentil (Lens esculentus)-specific Rhizobium sp. strain MRL3. Ecotoxicology 20:661–669

    Article  CAS  Google Scholar 

  • Ahemad M, Khan MS (2011c) Effect of pesticides on plant growth promoting traits of greengram-symbiont, Bradyrhizobium sp. strain MRM6. Bull Environ Contam Toxicol 86:384–388

    Article  CAS  Google Scholar 

  • Alexander DB, Zuberer DA (1991) Use of chrome azurol S reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soils 12:39–45

    Article  CAS  Google Scholar 

  • Barbosa HR, Thuler DS, Shirakawa MA, Miyasaka NRS (2000) Beijerinckia derxii stimulates the viability of non-N2-fixing bacteria in nitrogen-free media. Braz J Microbiol 31:168–173

    Article  CAS  Google Scholar 

  • Batista Filho A, Almeida JEM, Lamas C (2001) Effect of thiamethoxam on entomopathogenic microorganisms. Neotrop Entomol 30:437–447

    Article  CAS  Google Scholar 

  • Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 57:535–538

    CAS  Google Scholar 

  • Calafiori MH, Barbieri AA (2001) Effects of seed treatment with insecticide on the germination, nutrients, nodulation, yield and pest control in bean (Phaseolus vulgaris L.) culture. Ecossistema 26:97–104

    Google Scholar 

  • Casida JE (2011) Neonicotinoid metabolism: compounds, substituents, pathways, enzymes, organisms, and relevance. J Agric Food Chem 59:2923–2931

    Article  CAS  Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Bena G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  CAS  Google Scholar 

  • Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105

    Article  CAS  Google Scholar 

  • Ford KA, Casida JE (2006) Unique and common metabolites of thiamethoxam, clothianidin, and dinotefuran in mice. Chem Res Toxicol 19:1549–1556

    Article  CAS  Google Scholar 

  • Ford KA, Casida JE (2008) Comparative metabolism and pharmacokinetics of seven neonicotinoid insecticides in spinach. J Agric Food Chem 56:10168–10175

    Article  CAS  Google Scholar 

  • Ford KA, Casida JE, Chandran D, Gulevich AG, Okrent RA, Durkin KA, Sarpong R, Bunnelle EM, Wildermuth MC (2010) Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc Natl Acad Sci U S A 107:17527–17532

    Article  CAS  Google Scholar 

  • Gholami A, Shahsavani S, Nezarat S (2009) The effect of plant growth promoting rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int J Biol Life Sci 1:35–40

    Google Scholar 

  • Gupta S, Gajbhiye VT, Gupta RK (2008) Soil dissipation and leaching behavior of a neonicotinoid insecticide thiamethoxam. Bull Environ Contam Toxicol 80:431–437

    Article  CAS  Google Scholar 

  • Harada N, Takagi K, Baba K, Fujii K, Iwasaki A (2010) Biodegradation of diphenylarsinic acid to arsenic acid by novel soil bacteria isolated from contaminated soil. Biodegradation 21:491–499

    Article  CAS  Google Scholar 

  • Horii A, McCue P, Shetty K (2007) Enhancement of seed vigour following insecticide and phenolic elicitor treatment. Bioresour Technol 98:623–632

    Article  CAS  Google Scholar 

  • Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    Article  CAS  Google Scholar 

  • Kanne DB, Dick RA, Tomizawa M, Casida JE (2005) Neonicotinoid nitroguanidine insecticide metabolites: synthesis and nicotinic receptor potency of guanidines, aminoguanidines, and their derivatives. Chem Res Toxicol 18:1479–1484

    Article  CAS  Google Scholar 

  • Karmakar R, Singh SB, Kulshrestha G (2006) Persistence and transformation of thiamethoxam, a neonicotinoid insecticide, in soil of different agroclimatic zones of India. Bull Environ Contam Toxicol 76:400–406

    Article  CAS  Google Scholar 

  • Karmakar R, Bhattacharya R, Kulshrestha G (2009) Comparative metabolite profiling of the insecticide thiamethoxam in plant and cell suspension culture of tomato. J Agric Food Chem 57:6369–6374

    Article  CAS  Google Scholar 

  • Le Casida JR (1982) Ensifer adhaerens gen. nov., sp. nov. A bacterial predator of bacteria in soil. Int J Syst Bacteriol 32:339–345

    Article  Google Scholar 

  • Lei L, Zhang W, Wei H, Xia Z, Liu X (2009) Characterization of a novel nicotine-degrading Ensifer sp. strain N7 isolated from tobacco rhizosphere. Ann Microbiol 59:247–252

    Article  CAS  Google Scholar 

  • Liu Z, Dai Y, Huang G, Gu Y, Ni J, Wei H, Yuan S (2011) Soil microbial degradation of neonicotinoid insecticides imidacloprid, acetamiprid, thiacloprid and imidaclothiz and its effect on the persistence of bioefficacy against horsebean aphid Aphis craccivora Koch after soil application. Pest Manag Sci 67:1245–1252

    Article  CAS  Google Scholar 

  • Macedo WR, Castro PRC (2011) Thiamethoxam: molecule moderator of growth, metabolism and production of spring wheat. Pestic Biochem Physiol 100:299–304

    Article  CAS  Google Scholar 

  • Mody B, Bindra M, Modi V (1989) Extracellular polysaccharides of cowpea rhizobia: compositional and functional studies. Arch Microbiol 153:38–42

    Article  CAS  Google Scholar 

  • Myresiotis C, Vryzas Z, Papadopoulou-Mourkidou E (2011) Biodegradation of soil-applied pesticides by selected strains of plant growth-promoting rhizobacteria (PGPR) and their effects on bacterial growth. Biodegradation 23:297–310

    Article  Google Scholar 

  • Nauen R, Ebbinghaus-Kintscher U, Salgado VL, Kaussmann M (2003) Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic Biochem Physiol 76:55–69

    Article  CAS  Google Scholar 

  • Pandey G, Dorrian SJ, Russell RJ, Oakeshott JG (2009) Biotransformation of the neonicotinoid insecticides imidacloprid and thiamethoxam by Pseudomonas sp. 1 G. Biochem Biophys Res Commun 380:710–714

    Article  CAS  Google Scholar 

  • Reeves MW, Pine L, Neilands JB, Balows A (1983) Absence of siderophore activity in Legionella species grown in iron-deficient media. J Bacteriol 154:324–329

    CAS  Google Scholar 

  • Rogel MA, Hernandez-Lucas I, Kuykendall LD, Balkwill DL, Martinez-Romero E (2001) Nitrogen-fixing nodules with Ensifer adhaerens harboring Rhizobium tropici symbiotic plasmids. Appl Environ Microbiol 67:3264–3268

    Article  CAS  Google Scholar 

  • Sandhya V, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62:21–30

    Article  CAS  Google Scholar 

  • Schippers B, Bakker AW, Bakker P, Peer R (1990) Beneficial and deleterious effects of HCN-producing pseudomonads on rhizosphere interactions. Plant Soil 129:75–83

    Article  CAS  Google Scholar 

  • Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V (2009) Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasis-regulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol 85:371–381

    Article  CAS  Google Scholar 

  • Stefan M, Mihasan M, Dunca S (2008) Plant growth promoting rhizobacteria can inhibit the in vitro germination of Glycine max L. seeds. Scientific Annals of University “Alexandru Ioan Cuza” Iasi, Section Genetics and Molecular Biology, T. IX. 3:105–110

  • Weinert N, Meincke R, Gottwald C, Heuer H, Schloter M, Berg G, Smalla K (2010) Bacterial diversity on the surface of potato tubers in soil and the influence of the plant genotype. FEMS Microbiol Ecol 74:114–123

    Article  CAS  Google Scholar 

  • Wendt T, Doohan F, Mullins E (2011) Production of Phytophthora infestans-resistant potato (Solanum tuberosum) utilizing Ensifer adhaerens OV14. Transgenic Res 21:567–578

    Article  Google Scholar 

  • Yeager CM, Kornosky JL, Morgan RE, Cain EC, Garcia-Pichel F, Housman DC, Belnap J, Kuske CR (2007) Three distinct clades of cultured heterocystous cyanobacteria constitute the dominant N2-fixing members of biological soil crusts of the Colorado Plateau, USA. FEMS Microbiol Ecol 60:85–97

    Article  CAS  Google Scholar 

  • Yutani M, Taniguchi H, Borjihan H, Ogita A, Fujita K, Tanaka T (2011) Alliinase from Ensifer adhaerens and its use for generation of fungicidal activity. AMB Express 1:1–8

    Article  Google Scholar 

  • Zakhia F, Jeder H, Willems A, Gillis M, Dreyfus B, De Lajudie P (2006) Diverse bacteria associated with root nodules of spontaneous legumes in Tunisia and first report for nifH-like gene within the genera Microbacterium and Starkeya. Microb Ecol 51:375–393

    Article  Google Scholar 

  • Zhang X, Sun L, Qiu F, McLean RJC, Jiang R, Song W (2008) Rheinheimera tangshanensis sp. nov., a rice root-associated bacterium. Int J Syst Evol Microbiol 58:2420–2424

    Article  CAS  Google Scholar 

  • Zhang XX, Qiu FB, Sun L, Ma XT, Jiang RB, Song W (2010) Phylogenetic analysis of endophytic Ensifer adhaerens isolated from rice roots. Chin J Appl Environ Biol 16:779–783

    CAS  Google Scholar 

  • Zhou B, Yuan R, Shi C, Yu L, Gu J, Zhang C (2011) Biodegradation of geosmin in drinking water by novel bacteria isolated from biologically active carbon. J Environ Sci (China) 23:816–823

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was financed by the Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions, National Science Foundation of China (30970040), the National Science Fund for Talent Training in Basic Science (J1103507), and the Professional and Public Project of National Environmental Protection (201009033).

Author information

Authors and Affiliations

  1. Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Science, Nanjing Normal University, Nanjing, 210023, People’s Republic of China

    Guang-can Zhou, Ying Wang, Shan Zhai, Zhong-hua Liu, Yi-jun Dai, Sheng Yuan & Jun-yi Hou

  2. Nanjing Institute of Environmental Sciences, Ministry of Environmental Protection, Nanjing, 210042, People’s Republic of China

    Feng Ge

Authors
  1. Guang-can Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shan Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Feng Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhong-hua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yi-jun Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sheng Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jun-yi Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yi-jun Dai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, Gc., Wang, Y., Zhai, S. et al. Biodegradation of the neonicotinoid insecticide thiamethoxam by the nitrogen-fixing and plant-growth-promoting rhizobacterium Ensifer adhaerens strain TMX-23. Appl Microbiol Biotechnol 97, 4065–4074 (2013). https://doi.org/10.1007/s00253-012-4638-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4638-3

Keywords

Search

Navigation