Advertisement

Applied Microbiology and Biotechnology

, Volume 93, Issue 2, pp 787–796 | Cite as

Distribution of glyphosate and methylphosphonate catabolism systems in soil bacteria Ochrobactrum anthropi and Achromobacter sp

  • Alexey V. Sviridov
  • Tatyana V. Shushkova
  • Nina F. Zelenkova
  • Natalya G. Vinokurova
  • Igor G. Morgunov
  • Inna T. Ermakova
  • Alexey A. Leontievsky
Applied microbial and cell physiology

Abstract

Bacterial strains capable of utilizing methylphosphonic acid (MP) or glyphosate (GP) as the sole sources of phosphorus were isolated from soils contaminated with these organophosphonates. The strains isolated from MP-contaminated soils grew on MP and failed to grow on GP. One group of the isolates from GP-contaminated soils grew only on MP, while the other one grew on MP and GP. Strains Achromobacter sp. MPS 12 (VKM B-2694), MP degraders group, and Ochrobactrum anthropi GPK 3 (VKM B-2554D), GP degraders group, demonstrated the best degradative capabilities towards MP and GP, respectively, and were studied for the distribution of their organophosphonate catabolism systems. In Achromobacter sp. MPS 12, degradation of MP was catalyzed by C–P lyase incapable of degrading GP (C–P lyase I). Adaptation to growth on GP yielded the strain Achromobacter sp. MPS 12A, which retained its ability to degrade MP via C–P lyase I and was capable of degrading GP with formation of sarcosine, thus suggesting the involvement of a GP-specific C–P lyase II. O. anthropi GPK 3 also degraded MP via C–P lyase I, but degradation of GP in it was initiated by glyphosate oxidoreductase, which was followed by product transformation via the phosphonatase pathway.

Keywords

Phosphonates Glyphosate Methylphosphonic acid C–P lyase Glyphosate Oxidoreductase Phosphonatase 

Notes

Acknowledgements

This work was supported by the International Science and Technology Center (Grant No. 1892.2), the Russian Federal Agency for Education (Grant No. 2.1.1.9227), and the Russian Foundation for Basic Research (Project No. 09-04-00320).

References

  1. Adams MA, Luo Y, Hove-Jensen B, He SM, van Staalduinen LM, Zechel DL, Jia Z (2008) Crystal structure of PhnH: as essential component of carbon–phosphorus lyase in Escherichia coli. J Bacteriol 190:1072–1083CrossRefGoogle Scholar
  2. Balthazor TM, Hallas LE (1986) Glyphosate-degrading microorganisms from industrial activated sludge. Appl Environ Microbiol 51:432–434Google Scholar
  3. Dick RE, Quinn JP (1995) Glyphosate-degrading isolates from environmental samples: occurrence and pathways of degradation. Appl Microbiol Biotechnol 43:545–550CrossRefGoogle Scholar
  4. Ermakova IT, Shushkova TV, Leontievsky AA (2008) Microbial degradation of organophosphonates by soil bacteria. Microbiology (Moscow) 77:615–620CrossRefGoogle Scholar
  5. Ermakova IT, Kiseleva NI, Shushkova TV, Zharikov M, Zharikov GA, Leontievsky AA (2010) Bioremediation of glyphosate-contaminated soils. Appl Microbiol Biotechnol 88:585–594CrossRefGoogle Scholar
  6. Gard JK, Feng PCC, Hutton WC (1997) Nuclear magnetic resonance timecourse studies of glyphosate metabolism by microbial soil isolates. Xenobiotica 27:633–644CrossRefGoogle Scholar
  7. Hess HH, Derr JE (1975) Assay of inorganic and organic phosphorus in the 0.1–5 nanomole range. Anal Biochem 63:607–613CrossRefGoogle Scholar
  8. Hove-Jensen B, Rosenkrantz TJ, Haldimann A, Wanner BL (2003) Escherichia coli phnN, encoding ribose 1,5-bisphosphokinase activity (phosphoribosyl diphosphate forming): dual role in phosphonate degradation and NAD biosynthesis pathways. J Bacteriol 185:2793–2801CrossRefGoogle Scholar
  9. Hove-Jensen B, Rosenkrantz TJ, Zechel DL, Willemoës M (2010) Accumulation of intermediates of the carbon–phosphorus lyase pathway for phosphonate degradation in phn mutants of Escherichia coli. J Bacteriol 192:370–374CrossRefGoogle Scholar
  10. Isbell AF, Englert LF, Rosenberg H (1969) Phosphonoacetaldehyde. J Org Chem 34:755–756CrossRefGoogle Scholar
  11. Jacob GS, Garbow JR, Hallas LE, Kimack NM, Kishore GM, Schaefer J (1988) Metabolism of glyphosate in Pseudomonas sp. strain LBr. Appl Environ Microbiol 54:2953–2958Google Scholar
  12. Jiang WH, Metcalf WW, Lee KS, Wanner BL (1995) Molecular cloning, mapping, and regulation of Pho-regulon genes for phosphonate breakdown by the phosphonatase pathway of Salmonella typhimurium LT2. J Bacteriol 177:6411–6421Google Scholar
  13. Kertesz M, Elgorriaga A, Amrhein N (1991) Evidence for two distinct phosphonate-degrading enzymes (C–P lyases) in Arthrobacter sp. GLP-1. Biodegradation 2:53–59CrossRefGoogle Scholar
  14. Kim AD, Baker AS, Dunaway-Mariano D, Metcalf WW, Wanner BL, Martin BM (2002) The 2-aminoethylphosphonate-specific transaminase of the 2-aminoethylphosphonate degradation pathway. J Bacteriol 184:4134–4140CrossRefGoogle Scholar
  15. Kishore GM, Barry GF (1992) Glyphosate tolerant plants. International patent WO92/00377Google Scholar
  16. Kishore GM, Jacob GS (1987) Degradation of glyphosate by Pseudomonas sp. PG2982 via a sarcosine intermediate. J Biol Chem 262:12164–12168Google Scholar
  17. Kononova SV, Nesmeyanova MA (2002) Phosphonates and their degradation by microorganisms. Biochemistry (Moscow) 67:184–195CrossRefGoogle Scholar
  18. Lee KS, Metcalf WW, Wanner BL (1992) Evidence for two phosphonate degradative pathways in Enterobacter aerogenes. J Bacteriol 174:2501–2510Google Scholar
  19. Liu CM, McLean PA, Sookdeo CC, Cannon FC (1991) Degradation of the herbicide glyphosate by members of the family Rhizobiaceae. Appl Environ Microbiol 57:1799–1804Google Scholar
  20. McAuliffe KS, Hallas LE, Kulpa CF (1990) Glyphosate degradation by Agrobacterium radiobacter isolated from activated sludge. J Ind Microbiol 6:219–221CrossRefGoogle Scholar
  21. McGrath JW, Wisdom GB, McMullan G, Larkin MJ, Quinn JP (1995) The purification and properties of phosphonoacetate hydrolase, a novel carbon–phosphorus bond cleavage enzyme from Pseudomonas flourescens 23 F. Eur J Biochem 234:225–230CrossRefGoogle Scholar
  22. Morais MC, Zhang GF, Zhang WH, Olsen DB, Dunaway-Mariano D, Allen KN (2004) X-ray crystallographic and site-directed mutagenesis analysis of the mechanism of Shiff-base formation in phosphonoacetaldehyde hydrolase catalysis. J Biol Chem 279:9353–9361CrossRefGoogle Scholar
  23. Obojska A, Lejczak B, Kubrak M (1999) Degradation of phosphonates by Streptomyces isolates. Appl Microbiol Biotechnol 51:872–876CrossRefGoogle Scholar
  24. Pipke R, Amrhein N (1988) Isolation and characterization of a mutant of Arthrobacter sp. strain GLP-1 which utilizes the herbicide glyphosate as its sole source of phosphorus and nitrogen. Appl Environ Microbiol 54:2868–2870Google Scholar
  25. Pipke R, Amrhein N, Jacob GS, Schaefer J, Kishore GM (1987) Metabolism of glyphosate in an Arthrobacter sp. GLP-1. Eur J Biochem 165:267–273CrossRefGoogle Scholar
  26. Podzelinska K, He SM, Wathier M, Yakunin A, Proudfoot M, Hove-Jensen B, Zechel DL, Jia Z (2009) Structure of PhnP, a phosphodiesterase of the carbon–phosphorus lyase pathway for phosphonate degradation. J Biol Chem 284:17216–17226CrossRefGoogle Scholar
  27. Quinn JP, Kulakova AN, Cooley NA, McGrath JW (2007) New ways to break an old bond: the bacterial carbon–phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ Microbiol 9:2392–2400CrossRefGoogle Scholar
  28. Schowanek D, Verstraete W (1990) Phosphonate utilization by bacterial cultures and enrichments from environmental samples. Appl Environ Microbiol 56:895–903Google Scholar
  29. Shames SL, Wackett LP, LaBarge MS, Kuczkowski RL, Walsh CT (1987) Fragmentative and stereochemical isomerization probes for hemolytic carbon to phosphorus bond scission catalyzed by bacterial carbon–phosphorus lyase. Bioorg Chem 15:366–373CrossRefGoogle Scholar
  30. Talbot HW, Johnson LM, Munnecke DM (1984) Glyphosate utilization by Pseudomonas sp. and Alcaligenes sp. isolated from environmental sources. Curr Microbiol 10:255–260CrossRefGoogle Scholar
  31. Ternan NG, Quinn JP (1998) Phosphate starvation-independent 2-aminoethylphosphonic acid biodegradation in a newly isolated strain of Pseudomonas putida, NG2. Syst Appl Microbiol 21:346–352CrossRefGoogle Scholar
  32. Ternan NG, McGrath JW, McMullan G, Quinn JP (1998) Review: Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J Microbiol Biotechnol 14:635–647CrossRefGoogle Scholar
  33. Ternan NG, Hamilton JT, Quinn JP (2000) Initial in vitro characterization of phosphonopyruvate hydrolase, a novel phosphate starvation-independent carbon–phosphorus bond cleavage enzyme in Burkholderia cepacea Pal6. Arch Microbiol 173:35–41CrossRefGoogle Scholar
  34. White AK, Metcalf WW (2004) Two C–P lyase operons in Pseudomonas stutzeri and their roles in the oxidation of phosphonates, phosphite, and hypophosphite. J Bacteriol 186:4730–4739CrossRefGoogle Scholar
  35. White AK, Metcalf WW (2007) Microbial metabolism of reduced phosphorus compounds. Annu Rev Microbiol 61:379–400CrossRefGoogle Scholar
  36. Zboinska E, Maliszewska I, Leijczak B, Kafarski P (1992) Degradation of organophosphonates by Penicillium citrinum. Lett Appl Microbiol 15:356–358CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Alexey V. Sviridov
    • 1
  • Tatyana V. Shushkova
    • 1
  • Nina F. Zelenkova
    • 1
    • 2
  • Natalya G. Vinokurova
    • 1
  • Igor G. Morgunov
    • 1
  • Inna T. Ermakova
    • 1
    • 2
  • Alexey A. Leontievsky
    • 1
    • 2
    • 3
  1. 1.G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of SciencesPushchinoRussia
  2. 2.Pushchino State UniversityPushchinoRussia
  3. 3.IBPM RASPushchinoRussia

Personalised recommendations