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Phosphonoacetate biosynthesis: In vitro detection of a novel NADP+-dependent phosphonoacetaldehyde-oxidizing activity in cell-extracts of a marine Roseobacter

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Abstract

A novel phosphonoacetaldehyde-oxidizing activity was detected in cell-extracts of the marine bacterium Roseovarius nubinhibens ISM grown on 2-aminoethylphosphonic acid (2-AEP; ciliatine). Extracts also contained 2-AEP transaminase and phosphonoacetate hydrolase activities. These findings indicate the existence of a biological route from 2-AEP via phosphonoacetaldehyde for the production of phosphonoacetate, which has not previously been shown to be a natural product. The three enzymes appear to constitute a previously-unreported pathway for the mineralization of 2-AEP which is a potentially important source of phosphorus in the nutrient-stressed marine environment.

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References

  1. Quin, L.D., The Presence of Compounds with a Carbon-Phosphorus Bond in Some Marine Invertebrates, Biochemistry, 1965, vol. 4, pp. 324–330.

    Article  CAS  Google Scholar 

  2. Glonek, T., Henderson, T.O., Hilderbrand, R.L., and Myers, T.C., Biological Phosphonates — Determination by P-31 Nuclear Magnetic Resonance. Science, 1970, vol. 169 pp. 192–194.

    Article  PubMed  CAS  Google Scholar 

  3. Metcalf, W.W. and van der Donk, W.A., Biosynthesis of Phosphonic and Phosphinic Acid Natural Products, Annu. Rev. Biochem., 2009, vol. 78, pp 65–94.

    Article  PubMed  CAS  Google Scholar 

  4. Quinn, J.P., Kulakova, A.N., Cooley, N.A., and McGrath, J.W., New Ways to Break an Old Bond: the Bacterial Carbon-Phosphorus Hydrolases and Their Role in Biogeochemical Phosphorus Cycling, Environ. Microbiol., 2007, vol. 9, pp. 2392–2400.

    Article  PubMed  CAS  Google Scholar 

  5. Baker, A.S., Ciocci, M.J., Metcalf, W.W., Kim, J., Babbitt, P.C., Wanner, B.L., Martin, B.M., and Dunaway-Mariano, D., Insights into the Mechanism of Catalysis by the P-C Bond-Cleaving Enzyme Phosphonoacetaldehyde Hydrolase Derived from Gene Sequence Analysis and Mutagenesis, Biochemistry, 1998, vol. 37, pp. 9305–9315.

    Article  PubMed  CAS  Google Scholar 

  6. Jiang, W.H., Metcalf, W.W., Lee, K.S., and Wanner, B.L., Molecular-Cloning, Map**, and Regulation of pho Regulon Genes for Phosphonate Breakdown by the Phosphonatase Pathway of Salmonella typhimurium LT2, J. Bacteriol., 1995, vol. 177, pp. 6411–6421.

    PubMed  CAS  Google Scholar 

  7. Ternan, N.G., McGrath, J.W., McMullan, G., and Quinn, J.P., Organophosphonates: Occurrence, Synthesis and Biodegradation by Microorganisms, World J. Microb. Biot., 1998, vol. 14, pp. 635–647.

    Article  CAS  Google Scholar 

  8. Ternan, N.G. and Quinn, J.P., Phosphate Starvation-Independent 2-Aminoethylphosphonic Acid Biodegradation in a Newly Isolated Strain of Pseudomonas putida, NG2, Syst. Appl. Microbiol., 1998, vol. 21, pp. 346–352.

    PubMed  CAS  Google Scholar 

  9. Baumann, P. and Baumann L., The Marine Gram-Negative Eubacteria: Genera Photobacterium, Beneckea, Alteromonas, Pseudomonas, and Alcaligenes, in The Prokaryotes, Starr, M.P., Stolp, H., Truper, A., Balows, A., and Schlegel, H.G., Eds., Berlin, Springer, 1981, pp. 1302–1331.

    Google Scholar 

  10. Binks, P.R., French, C.E., Nicklin, S., and Bruce N.C., Degradation of Pentaerythritol Tetranitrate by Enterobacter cloacae PB2. Appl. Environ. Microbiol., 1996, vol. 62, pp. 1214–1219.

    PubMed  CAS  Google Scholar 

  11. Fiske, C.H. and Subbarow, Y., The Colorimetric Determination of Phosphorus, J. Biol. Chem., 1925, vol. 66, pp. 375–400.

    CAS  Google Scholar 

  12. McGrath, J.W., Wisdom, G.B., McMullan, G., Larkin, M.J., and Quinn, J.P., The Purification and Properties of Phosphonoacetate Hydrolase, a Novel Carbon-Phosphorus Bond-Cleavage Enzyme from Pseudomonas fluorescens, 23F. Eur. J. Biochem., 1995, vol. 234, pp. 225–230.

    Article  PubMed  CAS  Google Scholar 

  13. Bradford, M.M., A rapid and Sensitive Detection Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.

    Article  PubMed  CAS  Google Scholar 

  14. Toyama, S., New Assay Method of Gamma-Amino Acid Aminotransferase with ortho-aminobenzaldehyde, Agr. Biol. Chem., 1974, vol. 38, pp. 2263–2265.

    CAS  Google Scholar 

  15. Murphy, C.D., Moss, S.J., and O’Hagan, D. Isolation of an Aldehyde Dehydrogenase Involved in the Oxidation of Fluoroacetaldehyde to Fluoroacetate in Streptomyces cattleya, Appl. Environ. Microbiol., 2001, vol 67, pp. 4919–4921.

    Article  PubMed  CAS  Google Scholar 

  16. Denger, K., Weinitschke, S., Hollemeyer, K., and Cook, A.M., Sulfoacetate Generated by Rhodopseudomonas palustris from Taurine, Arch. Microbiol., 2004, vol. 182, pp. 254–258.

    Article  PubMed  CAS  Google Scholar 

  17. Krejcik, Z., Denger, K., Weinitschke, S., Hollemeyer, K., Paces, V., Cook, A.M., and Smits, T.H.M., Sulfoacetate Released during the Assimilation of Taurine-Nitrogen by Neptuniibacter caesariensis: Purification of Sulfoacetaldehyde Dehydrogenase, Arch. Microbiol., 2008, vol. 190, pp. 159–168.

    Article  PubMed  CAS  Google Scholar 

  18. Kulakova, A.N., Kulakov, L.A., Akulenko, N.V., Ksenzenko, V.N., Hamilton, J.T.G., and Quinn, J.P., Structural and Functional Analysis of the Phosphonoacetate Hydrolase (phnA) Gene Region in Pseudomonas fluorescens 23F, J. Bacteriol., 2001, vol. 183, pp. 3268–3275.

    Article  PubMed  CAS  Google Scholar 

  19. Kulakova, A.N., Kulakov, L.A., and Quinn, J.P. Cloning of the Phosphonoacetate Hydrolase Gene from Pseudomonas fluorescens 23F Encoding a New Type of Carbon-Phosphorus Bond Cleaving Enzyme and Its Expression in Escherichia coli and Pseudomonas putida, Gene, 1997, vol. 195, pp. 49–53.

    Article  PubMed  CAS  Google Scholar 

  20. Jendrossek, D., Steinbuchel, A., and Schlegel, H.G., Three Different Proteins Exhibiting NAD-Dependent Acetaldehyde Dehydrogenase-Activity from Alcaligenes eutrophus, Eur. J. Biochem 1987, vol. 167, pp. 541–548.

    Article  PubMed  CAS  Google Scholar 

  21. Muraoka, H., Watabe, Y., Ogasawara, N., and Takahashi, H., Purification and Properties of 5 NADP-Dependent Aldehyde Dehydrogenases from Aceto-bacter aceti, J. Ferment. Technol., 1980, vol. 58, pp. 501–507.

    CAS  Google Scholar 

  22. Schrader, T., Zarnt, G., and Andreesen, J.R., NAD(P)-Dependent Aldehyde Dehydrogenases Induced during Growth of Ralstonia eutropha Strain Bo on Tetrahydrofurfuryl Alcohol, J. Bacteriol., 2001, vol. 183, pp. 7408–7411.

    Article  PubMed  CAS  Google Scholar 

  23. Gilbert, J.A., Thomas, S., Cooley, N.A., Kulakova, A., Field, D., Booth, T., McGrath, J.W., Quinn, J.P., and Joint, I., Potential for Phosphonoacetate Utilization by Marine Bacteria in Temperate Coastal Waters, Environ. Microbiol., 2009, vol. 11, pp. 111–125.

    Article  PubMed  CAS  Google Scholar 

  24. Panas, P., Ternan, N.G., Dooley, J.S.G., and McMullan, G., Detection of Phosphonoacetate Degradation and phnA Genes in Soil Bacteria from Distinct Geographical Origins Suggest Its Possible Biogenic Origin, Environ. Microbiol., 2006, vol. 8, pp 939–945.

    Article  PubMed  CAS  Google Scholar 

  25. Thomas, S., Burdett, H., Temperton, B., Wick, R., Snelling, D., McGrath, J.W., Quinn, J.P., Munn, C., and Gilbert, J.A., Evidence for Phosphonate Usage in the Coral Holobiont, ISME J., 2010, vol. 4, pp. 459–461.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to J. W. McGrath.

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Cooley, N.A., Kulakova, A.N., Villarreal-Chiu, J.F. et al. Phosphonoacetate biosynthesis: In vitro detection of a novel NADP+-dependent phosphonoacetaldehyde-oxidizing activity in cell-extracts of a marine Roseobacter . Microbiology 80, 335–340 (2011). https://doi.org/10.1134/S0026261711030076

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