The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment

Frontiers in Microbiology

Volumn 3, Issue JAN, 2012, Pages

  Villarreal Chiu, Juan F ^a   Quinn, John P ^a   McGrath, John W ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

C P bond; Marine bacteria; Phosphonate; Phosphorus cycling

Indexed keywords

EID: 84875038227     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00019     Document Type: Article

References (88)

1. Agarwal, V., Borisova, S. A., Met-calf, W. W., van der Donk, W. A., and Nair, S. K. (2011). Structural and mechanistic insights into C-P bond hydrolysis by phosphonoacetate hydrolase. Chem. Biol. 18, 1230-1240.
2. Baker, A. S., Ciocci, M. J., Metcalf, W. W., Kim, J., Babbitt, P. C., Wanner, B. L., Martin, B. M., and Dunaway-Mariano, D. (1998). Insights into the mechanism of catalysis by the P-C bond-cleaving enzyme phosphonoacetaldehyde hydrolase derived from gene sequence analysis and mutagenesis. Biochemistry 37, 9305-9315.
3. Barry, R. J., Bowman, E., McQueney, M., and Dunaway-Mariano, D. (1988). Elucidation of the 2-aminoethylphosphonate biosyn-thetic pathway in Tetrahymena pyriformis. Biochem. Biophys. Res. Commun. 153, 177-182.
4. Beier, D., and Gross, R. (2006). Regulation of bacterial virulence by two-component systems. Curr. Opin. Microbiol. 9, 143-152.
5. Benitez-Nelson, C. R., O'Neill, L., Kolowith, L. C., Pellechia, P., and Thunell, R. (2004). Phosphonates and particulate organic phosphorus cycling in an anoxic marine basin. Limnol. Oceanogr. 49, 1593-1604.
6. Beversdorf, L. J., White, A. E., Björk-man, K. M., Letelier, R. M., and Karl, D. M. (2010). Phosphonate metabolism of Trichodesmium IMS101 and the production of greenhouse gases. Limnol. Oceanogr. 55, 1768-1778.
7. Björkman, K. M., and Karl, D. M. (2003). Bioavailability of dissolved organic phosphorus in the euphotic zone at Station ALOHA, North Pacific Subtropical Gyre. Limnol. Oceanogr. 48, 1049-1057.
8. Borisova, S. A., Christman, H. D., Metcalf, M. E. M., Zulkepli, N. A., Zhang, J. K., van der Donk, W. A., and Metcalf, W W (2011). Genetic and biochemical characterization of a pathway for the degradation of 2-aminoethylphosphonate in Sinorhizobium meliloti 1021. J. Biol. Chem. 286, 22283-22290.
9. Bowman, E., McQueney, M., Barry, R. J., and Dunaway-Mariano, D. (1988). Catalysis and thermodynamics of the phos-phoenolpyruvate/phosphopyruvate rearrangement. Entry into the phosphonate class of naturally occurring organophosphorus compounds. J. Am. Chem. Soc. 110, 5575-5576.
10. Bury-Mone, S., Nomane, Y., Reymond, N., Barbet, R., Jacquet, E., Imbeaud, S., Jacq, A., and Bouloc, P. (2009). Global analysis of extracytoplas-mic stress signaling in Escherichia coli. PLoS Genet. 5, e1000651. doi:10.1371/journal.pgen.1000651.
11. Chen, C. C., Han, Y., Niu, W., Kulakova, A. N., Howard, A., Quinn, J. P., Dunaway-Mariano, D., and Herzberg, O. (2006). Structure and kinetics of phosphonopyru-vate hydrolase from Variovorax sp. Pal2: new insight into the divergence of catalysis within the PEP mutase/isocitrate lyase superfamily. Biochemistry 45, 11491-11504.
12. Choi, K. Y., Kim, D., Chae, J. C., Zyl-stra, G. J., and Kim, E. (2007). Requirement of duplicated operons for maximal metabolism of phtha-late by Rhodococcus sp. strain DK17. Biochem. Biophys. Res. Commun. 357, 766-771.
13. Circello, B. T., Eliot, A. C., Lee, J. H., van der Donk, W. A., and Metcalf, W. W (2010). Molecular cloning and heterologous expression of the dehydrophos biosyn-thetic gene cluster. Chem. Biol. 17, 402-411.
14. Cirz, R. T., O'Neill, B. M., Hammond, J. A., Head, S. R., and Romesberg, F. E. (2006). Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J. Bacteriol. 188, 7101-7110.
15. Clark, L. L., Ingall, E. D., and Ben-ner, R. (1998). Marine phosphorus is selectively remineralized. Nature 393, 426-426.
16. Cooley, N. A., Kulakova, N. A., Villarreal-Chiu, J. F., Gilbert, J. A., McGrath, J. W., and Quinn, J. P. (2011). Phosphonoacetate biosynthesis: in vitro detection of a novel NADP+-dependent phosphonoacetaldehyde-oxidizing activity in cell-extracts of a marine Roseobacter. Microbiology 80, 335-340.
17. Dumora, C., Lacoste, A. M., and Cassaigne, A. (1989). Phospho-noacetaldehyde hydrolase from Pseudomonas aeruginosapurification, properties and comparison with Bacillus cereus enzyme. Biochim. Biophys. Acta 997, 193-198.
18. Dyhrman, S., Ammerman, J. W., and Van Mooy, B. A. (2007). Microbes and the marine phosphorus cycle. Oceanography 20, 110-116.
19. Dyhrman, S., Chappell, P. D., Haley, S. T., Moffett, J. W., Orchard, E. D., Waterbury, J. B., and Webb, E. A. (2006). Phosphonate utilization by the globally important marine dia-zotroph Trichodesmium. Nature 439, 68-71.
20. Dyhrman, S., and Haley, S. (2006). Phosphorus scavenging in the unicellular marine diazotroph Cro-cosphaera watsonii. Appl. Environ. Microbiol. 72, 1452-1458.
21. Dyhrman, S. T., Benitez-Nelson, C. R., Orchard, E. D., Haley, S. T., and Pellechia, P. J. (2009). A micro-bial source of phosphonates in oligotrophic marine systems. Nat. Geosci. 2, 696-699.
22. Ford, J. L., Kaakoush, N. O., and Mendz, G. L. (2010). Phosphonate metabolism in Helicobacter pylori. Antonie Van Leeuwenhoek 97, 51-60.
23. Gebhard, S., and Cook, G. M. (2008). Differential regulation of high-affinity phosphate transport systems of Mycobacterium smegmatis: identification of PhnF, a repressor of the phnDCE operon. J. Bacteriol. 190, 1335-1343.
24. Gilbert, J. A., Thomas, S., Cooley, N. A., Kulakova, A., Field, D., Booth, T., McGrath, J. W., Quinn, J. P., and Joint, I. (2009). Potential for phosphonoacetate utilization by marine bacteria in temperate coastal waters. Environ. Microbiol. 11, 111-125.
25. Gomez-Garcia, M. R., Davison, M., Blain-Hartnung, M., Grossman, A. R., andBhaya, D. (2011). Alternative pathways for phosphonate metabolism in thermophilic cyanobacte-ria from microbial mats. ISME J. 5, 141-149.
26. Hilderbrand, R. L. (1983). The Role of Phosphonates in Living Systems. Boca Raton, FL: CRC Press Inc.
27. Hori, T., Horiguchi, M., and Hayashi, A. (1984). Biochemistry of Natural C-P Compounds. Kyoto: Maruzen Ltd.
28. Horigane, A., Horiguchi, M., and Mat-sumoto, T. (1989). Metabolism of 2-amino-3-phosphono [3-14C] pro-pionic acid in cell-free preparations of Tetrahymena. Biochim. Biophys. Acta 618, 383-388.
29. Hove-Jensen, B., McSorley, F. R., and Zechel, D. L. (2011). Physiological role of PhnP-specified phos-phoribosyl cyclic phosphodiesterase in catabolism of organophospho-nic acids by the carbon-phosphorus lyase pathway. J. Am. Chem. Soc. 133, 3617-3624.
30. Hove-Jensen, B., Rosenkrantz, T. J., Zechel, D. L., and Willemoës, M. (2010). Accumulation of intermediates of the carbon-phosphorus lyase pathway for phosphonate degradation in phn mutants of Escherichia coli. J. Bacteriol. 192, 370-374.
31. Huang, J., Su, Z., and Xu, Y. (2005). The evolution of microbial phosphonate degradative pathways. J. Mol. Evol. 61, 682-690.
32. Ilikchyan, I. N., McKay, R. M., Zehr, J. P., Dyhrman, S. T., and Bullerjahn, G. S. (2009). Detection and expression of the phosphonate transporter gene phnD in marine and freshwater pic-ocyanobacteria. Environ. Microbiol. 11, 1314-1324.
33. Jiang, W. H., Metcalf, W. W., Lee, K. S., and Wanner, B.L. (1995). Molecular cloning, mapping, and regulation of Pho regulon genes for phosphonate breakdown by the phosphonatase pathway of Salmonella typhimurium LT2. J. Bacteriol. 177, 6411-6421.
34. Jochimsen, B., Lolle, S., McSorley, F. R., Nabi, M., Stougaard, J., Zechel, D. L., and Hove-Jensen, B. (2011). Five phosphonate operon gene products as components of a multi-subunit complex of the carbon-phosphorus lyase pathway. Proc. Natl. Acad. Sci. U.S.A. 108, 11393-11398.
35. Johannes, T. W., DeSieno, M. A., Griffin, B. M., Thomas, P. M., Kelleher, N. L., Metcalf, W. W., and Zhao, H. (2010). Deciphering the late biosyn-thetic steps of antimalarial compound FR-900098. Chem. Biol. 17, 57-64.
36. Kamat, S. S., Williams, H. J., and Raushel, F. M. (2011). Intermediates in the transformation of phosphonates to phosphate by bacteria. Nature 480, 570-573.
37. Karl, D. M., Beversdorf, L. J., Björkman, K. M., Church, M. J., Martinez, A., and DeLong, E. F. (2008). Aerobic production of methane in the sea. Nat. Geosci. 1, 473-478.
38. Karl, D. M., Björkman, K. M., Dore, J. E., Fujieki, L., Hebel, D. V., Houlihan, T., Letelier, R. M., and Tupas, L. M. (2001). Ecological nitrogen-to-phosphorus stoichiometry at station ALOHA. Deep Sea Res. II 48, 1449-1470.
39. Kertesz, M., Elgorriaga, A., and Amrhein, N. (1991). Evidence for two distinct phosphonate-degrading enzymes (C-P lyases) in Arthrobacter sp. GLP-1. Biodegradation 2, 53-59.
40. Kim, A., Benning, M. M., OkLee, S., Quinn, J. P., Martin, B. M., Holden, H. M., and Dunaway-Mariano, D. (2011). Divergence of chemical function in the alkaline phosphatase superfamily: structure and mechanism of the C-P bond cleaving enzyme phosphonoacetate hydrolase. Biochemistry 50, 3481-3494.
41. Kim, A. D., Baker, A. S., Dunaway-Mariano, D., Metcalf, W W, Wanner, B. L., and Martin, B. M. (2002). The 2-aminoethylphosphonate-specific transaminase of the 2-aminoethylphosphonate degradation pathway. J. Bacteriol. 184, 4134-4140.
42. Kittredge, J. S., and Hughes, R. R. (1964). The occurrence of alpha-amino-beta-phosphonopropionic acid in the Zoanthid, Zoanthus sociatus, and the ciliate, Tetrahymena pyriformis. Biochemistry 3, 991-996.
43. Kolowith, L. C., Ingall, E. D., and Benner, R. (2001). Composition and cycling of marine organic phosphorus. Lim-nol. Oceanogr. 46, 309-320.
44. Kulakova, A. N., Kulakov, L. A., Aku-lenko, N. V., Ksenzenko, V N., Hamilton, J. T. G., and Quinn, J. P. (2001). Structural and functional analysis of the phosphonoacetate hydrolase (phnA) gene region in Pseudomonas fluorescens 23F. J. Bacteriol. 183, 3268-3275.
45. Kulakova, A. N., Kulakov, L. A., McGrath, J. W., and Quinn, J. P. (2009). The construction of a whole-cell biosensor for phosphonoacetate, based on the LysR-like transcriptional regulator PhnR from Pseudomonas fluorescens 23F. Microb. Biotechnol. 2, 234-240.
46. Kulakova, A. N., Wisdom, G. B., Kulakov, L. A., and Quinn, J. P. (2003). The purification and characterization of phosphonopy-ruvate hydrolase, a novel carbon-phosphorus bond cleavage enzyme from Variovorax sp. Pal2. J. Biol. Chem. 278, 23426-23431.
47. Kuwahara, T., Yamashita, A., Hirakawa, H., Nakayama, H., Toh, H., Okada, N., Kuhara, S., Hattori, M., Hayashi, T., and Ohnishi, Y. (2004). Genomic analysis of Bacteroidesfragilis reveals extensive DNA inversions regulating cell surface adaptation. Proc. Natl. Acad. Sci. U.S.A. 101, 14919-14924.
48. Lamarche, M. G., Wanner, B. L., Cre-pin, S., and Harel, J. (2008). The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 32, 461-473.
49. LaNauze, J. M., Coggins, J. R., and Dixon, H. B. F. (1977). Aldolase-like imine formation in mechanism of action of phosphonoacetalde-hyde hydrolase. Biochem. J. 165, 409-411.
50. Lee, J. H., Bae, B., Kuemin, M., Circello, B. T., Metcalf, W. W., Nair, S. K., and van der Donk, W A. (2010). Characterization and structure of DhpI, a phosphonate O-methyltransferase involved in dehydrophos biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 107, 17557-17562.
51. Lim, B. L., Yeung, P., Cheng, C., and Hill, J. E. (2007). Distribution and diversity of phytate-mineralizing bacteria. ISMEJ. 1, 321-330.
52. Luo, H., Benner, R., Long, R. A., and Hu, H. (2009). Subcellular localization of marine bacterial alkaline phos-phatases. Proc. Natl. Acad. Sci. U.S.A. 106, 21219-21233.
53. Luo, H., Zhang, H., Long, R. A., and Benner, R. (2011). Depth distributions of alkaline phosphatase and phosphonate utilization genes in the North Pacific Subtropical Gyre. Aquat. Microb. Ecol. 62, 61-69.
54. Martinez, A., Tyson, G. W., and DeLong, E. F. (2010). Widespread known and novel phosphonate utilization pathways in marine bacteria revealed by functional screening and metage-nomic analyses. Environ. Microbiol. 12, 222-238.
55. McGrath, J. W., Hammerschmidt, F., Kählig, H., Wuggenig, F., Lamprecht, G., and Quinn, J. P. (2011). Studies on the biodegradation of fos-fomycin: synthesis of (13) C-labeled intermediates, feeding experiments with Rhizobium huakuii PMY1, and isolation of labeled amino acids from cell mass by HPLC. Chemistry 17, 13341-13348.
56. McGrath, J. W., Hammerschmidt, F., Preusser, W., Quinn, J. P., and Schweifer, A. (2009). Studies on the biodegradation of fosfomycin: growth of Rhizobium huakuii PMY1 on possible intermediates synthe-sised chemically. Org. Biomol Chem. 7, 1944-1953.
57. McGrath, J. W., Hammerschmidt, E, and Quinn, J. P. (1998). Biodegradation of phosphonomycin by Rhizobium huakuii PMY1. Appl. Environ. Microbiol. 64, 356-358.
58. McGrath, J. W., Ternan, N. G., and Quinn, J. P. (1997). Utilization of organophosphonates by environmental microorganisms. Lett. Appl. Microbiol. 24, 69-73.
59. McGrath, J. W., Wisdom, G. B., McMul-lan, G., Larkin, M. J., and Quinn, J. P. (1995). The purification and properties of phosphonoacetate hydrolase, a novel carbon-phosphorus bond cleavage enzyme from Pseudomonas fluorescens. Eur. J. Biochem. 234, 225-230.
60. McMullan, G., Harrington, F., and Quinn, J. P. (1992). Metabolism of phosphonoacetate as the sole carbon and phosphorus source by an environmental bacterial isolate. Appl. Environ. Microbiol. 58, 1364-1366.
61. Mendz, G. L., Mégraud, F., and Koro-lik, V. (2005). Phosphonate catab-olism by Campylobacter spp. Arch. Microbiol. 183, 113-120.
62. Metcalf, W. W., and van der Donk, W. A. (2009). Biosynthesis of phos-phonic and phosphinic acid natural products. Annu. Rev. Biochem. 78, 65-94.
63. Morais, M. C., Zhang, G. F., Zhang, W. H., Olsen, D. B., Dunaway-Mariano, D., and Allen, K. N. (2004). X-ray crystallographic and site-directed mutagenesis analysis of the mechanism of Schiff-base formation in phosphonoacetaldehyde hydrolase catalysis. J. Biol. Chem. 279, 9353-9361.
64. Moran, M. A., Belas, R., Schell, M. A., González, J. M., Sun, F., Sun, S., Binder, B. J., Edmonds, J., Ye, W., Orcutt, B., Howard, E. C., Meile, C., Palefsky, W., Goesmann, A., Ren, Q., Paulsen, I., Ulrich, L. E., Thompson, L. S., Saunders, E., and Buchan, A. (2007). Ecological genomics of marine Roseobacters. Appl. Environ. Microbiol. 73, 4559-4569.
65. Moran, M. A., Buchan, A., Gonzalez, J. M., Heidelberg, J. F., Whitman, W B., Kiene, R. P., Henriksen, J. R., King, G. M., Belas, R., Fuqua, C., Brinkac, L., Lewis, M., Johri, S., Weaver, B., Pai, G., Eisen, J. A., Rahe, E., Sheldon, W. M., Ye, W., Miller, T. R., Carlton, J., Rasko, D. A., Paulsen, I. T., Ren, Q., Daugherty, S. C., Deboy, R. T., Dodson, R. J., Durkin, A. S., Madupu, R., Nelson, W. C., Sullivan, S. A., Rosovitz, M. J., Haft, D. H., Selengut, J., and Ward, N. (2004). Genome sequence of Silicibacterpomeroyi reveals adaptations to the marine environment. Nature 432, 910-913.
66. Nealson, K. H., and Venter, J. C. (2007). Metagenomics and the global ocean survey: what's in it for us, and why should we care? ISMEJ. 1, 185-190.
67. Palenik, B., Brahamsha, B., Larimer, F. W., Land, M., Hauser, L., Chain, P., Lamerdin, J., Regala, W., Allen, E. E., McCarren, J., Paulsen, I., Dufresne, A., Partensky, F., Webb, E. A., and Waterbury, J. (2003). The genome of a motile marine Synechococcus. Nature 424, 1037-1042.
68. Paytan, A., and McLaughlin, A. (2007). The oceanic phosphorus cycle. Chem. Rev. 107, 563-576.
69. Quin, L. D. (1965). The presences of compounds with a carbon-phosphorus bond in some marine invertebrates. Biochemistry 4, 324-330.
70. Quin, L. D. (2000). A Guide to Organophosphorus Chemistry. New York: John Wiley & Sons.
71. Quin, L. D., and Quin, G. S. (2001). Screening for carbon-bound phosphorus in marine animals by high-resolution P-31 NMR spectroscopy: coastal and hydrothermal vent invertebrates. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 128, 173-185.
72. Quinn, J. P., Kulakova, A. N., Cooley, N. A., and McGrath, J. W. (2007). New ways to break an old bond: the bacterial carbon-phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ. Microbiol. 9, 2392-2400.
73. Rizk, S.S., Cuneo, M.J., and Hellinga, H. W. (2006). Identification of cognate ligands for the Escherichia coli phnD protein product and engineering of a reagentless fluorescent biosensor for phosphonates. Protein Sci. 15, 1745-1751.
74. Seidel, H. M., Freeman, S., Seto, H., and Knowles, J. R. (1988). Phosphonate biosynthesis: isolation of the enzyme responsible for the formation of a carbon-phosphorus bond. Nature 335, 457-458.
75. Sowell, S. M., Wilhelm, L. J., Norbeck, A. D., Lipton, M. S., Nicora, C. D., Barofsky, D. F., Carlson, C. A., Smith, R. D., and Giovanonni, S. J. (2009). Transport functions dominate the SAR1 1 metaproteome at low-nutrient extremes in the Sargasso Sea. ISMEJ. 3, 93-105.
76. Sviridov, A. V., Shushkova, T. V., Zelenkova, N. F., Vinokurova, N. G., Morgunov, I. G., Ermakova, I. T., and Leontievsky, A. A. (2012). Distribution of glyphosate and methylphos-phonate catabolism systems in soil bacteria Ochrobactrum anthropi and Achromobacter sp. Appl. Microbiol. Biotechnol. 93, 787-796.
77. Ternan, N. G., McGrath, J. W., McMullan, G., and Quinn, J. P. (1998). Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J. Microbiol. Biotechnol. 14, 635-647.
78. Ternan, N. G., and Quinn, J. P. (1998a). Phosphate starvation-independent 2-aminoethylphosphonic acid biodegradation in a newly isolated strain of Pseudomonas putida, NG2. Syst. Appl. Microbiol. 21, 346-352.
79. Ternan, N. G., and Quinn, J. P. (1998b). In vitro cleavage of the carbon-phosphorus bond of phosphonopy-ruvate by cell extracts of an environmental Burkholderia cepacia isolate. Biochem. Biophys. Res. Com-mun. 248, 378-381.
80. Thomas, S., Burdett, H., Temperton, B., Wick, R., Snelling, D., McGrath, J. W., Quinn, J. P., Munn, C., and Gilbert, J. A. (2010). Evidence for phosphonate usage in the coral holo-biont. ISMEJ. 4, 459-461.
81. Vera, M., Pagliai, F., Guiliani, N., and Jerez, C. A. (2008). The chemolithoautotroph Acidithiobacillus ferrooxidans can survive under phosphate-limiting conditions by expressing a C-P lyase operon that allows it to grow on phosphonates. Appl. Environ. Microbiol. 74, 1829-1835.
82. von Krüger, W. M., Humphreys, S., and Ketley, J. M. (1999). A role for the PhoBR regulatory system homologue in the Vibrio cholerae phosphate-limitation response and intestinal colonization. Microbiology 145, 2463-2475.
83. von Krüger, W. M., Lery, L. M. S., Soares, M. R., de Neves-Manta, F. S., Batista e Silva, C. M., Neves-Ferreira, A. G., Perales, J., and Bisch, P. M. (2006). The phosphate-starvation response in Vibrio cholerae O1 and a phoB mutant under proteomic analysis: disclosing functions involved in adaptation, survival and virulence. Proteomics6, 1495-1511.
84. Wackett, L. P., Shames, S. L., Ven-ditti, C. P., and Walsh, C. T. (1987). Bacterial carbon-phosphorus lyase-products, rates, and regulation of phosphonic and phosphinic acid metabolism. J. Bacteriol. 169, 710-717.
85. Wagner-Döbler, I., and Biebl, H. (2006). Environmental biology of the marine Roseobacter lineage. Annu. Rev. Microbiol. 60, 255-280.
86. White, A. K., and Metcalf, W.W (2007). Microbial metabolism of reduced phosphorus compounds. Annu. Rev. Microbiol. 61, 379-400.
87. Yakovleva, G. M., Kim, S. K., and Wanner, B. L. (1998). Phosphate-independent expression of the carbon-phosphorus lyase activity of Escherichia coli. Appl. Microbiol. Biotechnol. 49, 573-578.
88. Zhang, G., Dai, J., Lu, Z., and Dunaway-Mariano, D. (2003). The phospho-nopyruvate decarboxylase from Bac-teroides fragilis. J. Biol. Chem. 278, 41302-41308.