Skip to main content
Log in

Biodegradation of Organophosphorus Pollutants by Soil Bacteria: Biochemical Aspects and Unsolved Problems

  • BIOTECHNOLOGICAL METHODS IN ECOLOGY
  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

The degradation of stable organophosphorus pollutants has been studied in six soil bacterial isolates and three strains of bacteria adapted to utilize glyphosate herbicide (GP) under laboratory conditions. Significant differences in the uptake of organophosphonates were found in taxonomically close strains possessing similar enzymatic pathways of catabolism of these compounds, which suggests the existence of unknown mechanisms for the regulation of the activity of these enzymes. The effect of adaptation to GP utilization as the sole phosphorus source on the consumption rates of several other structurally different phosphonates was observed in the studied bacteria. New, highly efficient degrading strains that resulted in a GP decomposition of up to 56% after soil application were isolated. Unsolved problems of microbial GP metabolism and trends in further research on the creation of effective preparations for the bioremediation of soils contaminated with organophosphonates are discussed.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. White, A.K. and Metcalf, W.W., Microbial metabolism of reduced phosphorus compounds, Annu. Rev. Microbiol., 2007, vol. 61, pp. 379–400. https://doi.org/10.1146/annurev.micro.61.080706.093357

    Article  CAS  PubMed  Google Scholar 

  2. McGrath, J.W., Chin, J.P., and Quinn, J.P., Organophosphonates revealed: new insights into the microbial metabolism of ancient molecules, Nat. Rev. Microbiol., 2013, vol. 11, no. 6, pp. 412–419.

    Article  CAS  Google Scholar 

  3. Ermakova, I.T., Shushkova, T.V., and Leont’evskii, A.A., Microbial degradation of organophosphonates by soil bacteria, Microbiology (Moscow), 2008, vol. 77, pp. 615–620.

    Article  CAS  Google Scholar 

  4. Horsman, G.P. and Zechel, D.L., Phosphonate biochemistry, Chem. Rev., 2017, vol. 117, no. 8, pp. 5704–5783. https://doi.org/10.1021/acs.chemrev.6b00536

    Article  CAS  PubMed  Google Scholar 

  5. Benbrook, C.M., Trends in glyphosate herbicide use in the United States and globally, Environ. Sci. Eur., 2016, vol. 28, no. 3, pp. 1–15. https://doi.org/10.1186/s12302-016-0070-0

    Article  CAS  Google Scholar 

  6. Kniss, A.R., Long-term trends in the intensity and relative toxicity of herbicide use, Nat. Commun., 2017, vol. 8, p. 14865. https://doi.org/10.1038/ncomms14865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mesnag,e, R., Defarge, N., Spiroux de Vendomois, J., and Seralini, G.E., Potential toxic effects of glyphosate and its commercial formulations below regulatory limits, Food Chem. Toxicol., 2015, vol. 84, pp. 133–153. https://doi.org/10.1016/j.fct.2015.08.012

  8. Bai, S.H. and Ogbourne, S.M., Glyphosate: environmental contamination, toxicity and potential risks to human health via food contamination, Environ. Sci. Pollut. Res. Int., 2016, vol. 23, no. 19, pp. 18988–19001. https://doi.org/10.1007/s11356-016-7425-3

    Article  CAS  PubMed  Google Scholar 

  9. Zhan, H., Feng, Y., Fan, X., and Chen, S., Recent advances in glyphosate biodegradation, Appl. Microbiol. Biotechnol., 2018, vol. 102, no. 12, pp. 5033–5043. https://doi.org/10.1007/s00253-018-9035-0

    Article  CAS  PubMed  Google Scholar 

  10. Sviridov, A.V., Epiktetov, D.O., Shushkova, T.V., et al., Fosfororganicheskie neirotoksiny (Organophosphate Neurotoxins), Moscow: RIOR, 2020.

  11. Fan, J., Yang, G., Zhao, H., et al., Isolation, identification and characterization of a glyphosate-degrading bacterium, Bacillus cereus CB4, from soil, J. Gen. Appl. Microbiol., 2012, vol. 58, no. 4, pp. 263–271. https://doi.org/10.2323/jgam.58.263

    Article  CAS  PubMed  Google Scholar 

  12. Yu, X.M., Yu, T., Yin, G.H., et al., Glyphosate biodegradation and potential soil bioremediation by Bacillus subtilis strain Bs-15, Genet. Mol. Res., 2015, vol. 14, no. 4, pp. 14717–14730. https://doi.org/10.4238/2015

    Article  PubMed  Google Scholar 

  13. Huntscha, S., Stravs, M.A., Buhlmann, A., et al., Seasonal dynamics of glyphosate and AMPA in lake Greifensee: rapid microbial degradation in the epilimnion during summer, Environ. Sci. Technol., 2018, vol. 52, no. 8, pp. 4641–4649. https://doi.org/10.1021/acs.est.8b00314

    Article  CAS  PubMed  Google Scholar 

  14. Acosta-Cortés, A.G., Martinez-Ledezma, C., López-Chuken, U.J., et al., Polyphosphate recovery by a native Bacillus cereus strain as a direct effect of glyphosate uptake, ISME J., 2019, vol. 13, no. 6, pp. 1497–1505. https://doi.org/10.1038/s41396-019-0366-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ermakova, I.T. Kiseleva, N.I., et al., Bioremediation of glyphosate-contaminated soils, Appl. Microbiol. Biotechnol., 2010, vol. 88, no. 2, pp. 585–594. https://doi.org/10.1007/s00253-010-2775-0

    Article  CAS  PubMed  Google Scholar 

  16. Hove-Jensen, B., Zechel, D.L., and Jochimsen, B., Utilization of glyphosate as phosphate source: biochemistry and genetics of bacterial carbon-phosphorus lyase, Microbiol. Mol. Biol. Rev., 2014, vol. 78, no. 1, pp. 176–197. https://doi.org/10.1128/MMBR.00040-13

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lyagin, I.V., Andrianova, M.S., and Efremenko, E.N., Extensive hydrolysis of phosphonates as unexpected behavior of the known His6-organophosphorus hydrolase, Appl. Microbiol. Biotechnol., 2016, vol. 100, no. 13, pp. 5829–5838. https://doi.org/10.1007/s00253-016-7407-x

    Article  CAS  PubMed  Google Scholar 

  18. Villareal-Chiu, J.F., Quinn, J.P., and McGrath, J.W., The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment, Front. Microbiol., 2012, vol. 3, no. 19, pp. 1–13. https://doi.org/10.3389/fmicb.2012.00019

    Article  CAS  Google Scholar 

  19. Sosa, O.A., Repeta, D.J., DeLong, E.F., et al., Phosphate-limited ocean regions select for bacterial populations enriched in the carbon-phosphorus lyase pathway for phosphonate degradation, Environ. Microbiol., 2019, vol. 21, no. 7, pp. 2402–2414. https://doi.org/10.1111/1462-2920.14628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sviridov, A.V., Shushkova, T.V., Ermakova, I.T., et al., Microbial degradation of glyphosate herbicides (review), Appl. Biochem. Microbiol., 2015, vol. 51, no. 2, pp. 188–195.

    Article  CAS  Google Scholar 

  21. Kishore, G.M. and Barry, G.F., Glyphosate tolerant plants. US Patent no. US5463175A, 1995.

  22. Pedotti, M., Rosini, E., Molla, G., et al., Glyphosate resistance by engineering the flavoenzyme glycine oxidase, J. Biol. Chem., 2009, vol. 284, no. 51, pp. 36415–36423.

    Article  CAS  Google Scholar 

  23. Yao, P., Lin, Y., Wu, G., et al., Improvement of glycine oxidase by DNA shuffling, and site-saturation mutagenesis of F247 residue, Int. J. Biol. Macromol., 2015, vol. 79, pp. 965–970. https://doi.org/10.1016/j.ijbiomac.2015.05.030

    Article  CAS  PubMed  Google Scholar 

  24. Castle, L.A., Siehl, D.L., Gorton, R., et al., Discovery and directed evolution of a glyphosate tolerance gene, Science, 2004, vol. 304, no. 5674, pp. 1151–1154.

    Article  CAS  Google Scholar 

  25. Shushkova, T.V., Vinokurova, N.G., Baskunov, B.P., et al., Glyphosate acetylation as a specific trait of Achromobacter sp. Kg 16 physiology, Appl. Microbiol. Biotechnol., 2016, vol. 100, no. 2, pp. 847–855. https://doi.org/10.1007/s00253-015-7084-1

    Article  CAS  PubMed  Google Scholar 

  26. Kertesz, M., Elgorriaga, A., and Amrhein, N., Evidence for two distinct phosphonate-degrading enzymes (C-P lyases) in Arthrobacter sp. GLP-1, Biodegradation, 1991, vol. 2, no. 1, pp. 53–59. https://doi.org/10.1007/bf00122425

    Article  CAS  PubMed  Google Scholar 

  27. Sviridov, A.V., Shushkova, T.V., Zelenkova, N.F., et al., Distribution of glyphosate and methylphosphonate catabolism systems in soil bacteria Ochrobactrum anthropi and Achromobacter sp., Appl. Microbiol. Biotechnol., 2012, vol. 93, no. 2, pp. 787–796.

    Article  CAS  Google Scholar 

  28. Ermakova, I.T., Shushkova, T.V., Sviridov, A.V., et al., Organophosphonates utilization by soil strains of Ochrobactrum anthropi and Achromobacter sp., Arch. Microbiol., 2017, vol. 199, no. 5, pp. 665–675.

    Article  CAS  Google Scholar 

  29. Sviridov, A.V., Zelenkova, N.F., Vinokurova, N.G., et al., New approaches to identification and activity estimation of glyphosate degradation enzymes, Biochemistry (Moscow), 2011, vol. 76, no. 6, pp. 720–725. https://doi.org/10.1134/S0006297911060149

    Article  CAS  PubMed  Google Scholar 

  30. Spilker, T., Vandamme, P., and LiPuma, J.J., A multilocus sequence typing scheme implies population structure and reveals several putative novel Achromobacter species, J. Clin. Microbiol., 2012, vol. 50, no. 9, pp. 3010–3015. https://doi.org/10.1128/JCM.00814-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Spilker, T., Vandamme, P., and LiPuma, J.J., Identification and distribution of Achromobacter species in cystic fibrosis, J. Cyst. Fibros., 2013, vol. 12, no. 3, pp. 298–301. https://doi.org/10.1016/j.jcf.2012.10.002

    Article  CAS  PubMed  Google Scholar 

  32. Bolger, A.M., Lohse, M., and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 2014, vol. 30, no. 15, pp. 2214–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  Google Scholar 

  33. Bankevich, A., Nurk, S., Antipov, D., et al., SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J. Comput. Biol., 2012, vol. 19, no. 5, pp. 455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Tatusova, T., DiCuccio, M., Badretdin, A., et al., NCBI Prokaryotic genome annotation pipeline, Nucleic Acids Res., 2016, vol. 44, no. 14, pp. 6614–6624. https://doi.org/10.1093/nar/gkw569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Shushkova, T.V., Vasilieva, G.K., Ermakova, I.T., and Leontievsky, A.A., Sorption and microbial degradation of glyphosphate in soil suspensions, Appl. Biochem. Microbiol., 2009, vol. 45, no. 6, pp. 599–603. https://doi.org/10.1134/S0003683809060040

    Article  CAS  Google Scholar 

  36. Gimsing, A.L., Borggaard, O.K., Jacobsen, O.S., et al., Chemical and microbiological soil characteristics controlling glyphosate mineralization in Danish surface soils, Appl. Soil Ecol., 2004, vol. 27, no. 3, pp. 233–242. https://doi.org/10.1016/j.apsoil.2004.05.007

    Article  Google Scholar 

  37. Hadi, F., Mousavi, A., Noghabi, K.A., et al., New bacterial strain of the genus Ochrobactrum with glyphosate-degrading activity, J. Environ. Sci. Health B, 2013, vol. 48, no. 3, pp. 208–213. https://doi.org/10.1080/03601234.2013.730319

    Article  CAS  PubMed  Google Scholar 

  38. Firdous, S., Iqbal, S., Anwar, S., and Jabeen, H Identification and analysis of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene from glyphosate-resistant Ochrobactrum intermedium Sq20, Pest Manage. Sci., 2018, vol. 74, no. 5, pp. 1184–1196. https://doi.org/10.1002/ps.4624

    Article  CAS  Google Scholar 

  39. Bazot, S. and Lebeau, T., Simultaneous mineralization of glyphosate and diuron by a consortium of three bacteria as free-and/or immobilized-cells formulations, Appl. Microbiol. Biotechnol., 2008, vol. 77, no. 6, pp. 1351–1358. https://doi.org/10.1007/s00253-007-1259-3

    Article  CAS  PubMed  Google Scholar 

  40. Vandamme, P., Moore, E.R., Cnockaert, M., et al., Classification of Achromobacter genogroups 2, 5, 7 and 14 as Achromobacter insuavis sp. nov., Achromobacter aegrifaciens sp. nov., Achromobacter anxifer sp. nov. and Achromobacter dolens sp. nov., respectively, Syst. Appl. Microbiol., 2013, vol. 36, no. 7, pp. 474–482. https://doi.org/10.1016/j.syapm.2013.06.005

    Article  CAS  PubMed  Google Scholar 

  41. Zhang, G., Mazurkie, A.S., Dunaway-Mariano, D., and Allen, K.N., Kinetic evidence for a substrate-induced fit in phosphonoacetaldehyde hydrolase, Biochemistry, 2002, vol. 41, no. 45, pp. 13370–13377. https://doi.org/10.1021/bi026388n

    Article  CAS  PubMed  Google Scholar 

  42. Quinn, J.P., Kulakova, A.N., Cooley, N.A., and McGra-th, J.W., New ways to break an old bond: the bacterial carbonphosphorus hydrolases and their role in biogeochemical phosphorus cycling, Environ. Microbiol., 2007, vol. 9, no. 10, pp. 2392–2400. https://doi.org/10.1111/j.1462-2920.2007.01397.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The phosphonatase studies and whole genome sequencing were supported by the Russian Science Foundation, grant no. 18-074-00021.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. V. Sviridov.

Ethics declarations

The authors declare that they have no conflicts of interest.

This article does not contain any studies involving animals performed by any of the authors.

This article does not contain any studies involving human participants performed by any of the authors.

Additional information

Translated by I. Gordon

Abbreviations: 2-AEP—2-aminoethylphosphonate; AMPA—aminomethylphosphonic acid; CFU—colony-forming unit(s); dNTP—deoxyribonucleoside triphosphate; FMN—fosfomycin; GAT—glyphosate acetyl transferase; GOX—glyphosate oxidoreductase; GP—glyphosate; HPLC—high performance liquid chromatography; MLST—multilocus sequence typing; MPA—methylphosphonic acid; NADH—nicotinamide adenine dinucleotide (reduced); OP—organophosphonates; PA—phosphonoacetate; PAH—phosphonoacetate hydrolase; PCR—polymerase chain reaction; Pi—orthophosphate; PNT—phosphonatase (phosphonoacetaldehyde hydrolase).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sviridov, A.V., Shushkova, T.V., Epiktetov, D.O. et al. Biodegradation of Organophosphorus Pollutants by Soil Bacteria: Biochemical Aspects and Unsolved Problems. Appl Biochem Microbiol 57, 836–844 (2021). https://doi.org/10.1134/S0003683821070085

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0003683821070085

Keywords:

Navigation