Monofluorophosphate is a selective inhibitor of respiratory sulfate-reducing microorganisms

Environmental Science and Technology

Volumn 49, Issue 6, 2015, Pages 3727-3736

  Carlson, Hans K ^a   Stoeva, Magdalena K ^a   Justice, Nicholas B ^b   Sczesnak, Andrew ^c   Mullan, Mark R ^a   Mosqueda, Lorraine A ^a   Kuehl, Jennifer V ^b   Deutschbauer, Adam M ^b   Arkin, Adam P ^b,c   Coates, John D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c University of California   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INORGANIC COMPOUNDS; MICROBIOLOGY; MICROORGANISMS; NITRATES; REDUCTION; SELENIUM COMPOUNDS; SULFUR COMPOUNDS; TELLURIUM COMPOUNDS; TOXICITY;

EUKARYOTIC ORGANISMS; HIGH-THROUGHPUT ASSAYS; INDUSTRIAL OPERATIONS; MICROBIAL ECO SYSTEM; MONOFLUOROPHOSPHATE; POTENT INHIBITOR; SELECTIVE INHIBITORS; SULFATE REDUCTION;

CORROSION INHIBITORS;

CHALCOGEN; CHLORATE; FLUORIDE ION; FLUOROPHOSPHATE; HALOGEN; MOLYBDIC ACID; NITRATE; NITRITE; PERCHLORATE; SELENATE; SELENITE; SELENIUM; SODIUM; SULFATE; SULFATE ADENYLYLTRANSFERASE; SULFIDE; SULFITE; TELLURIUM DERIVATIVE; TUNGSTEN DERIVATIVE; VANADIC ACID; ANION; CHLORIDE; CHLORITE; FLUORIDE; ION; OXYGEN; PHOSPHATE;

CYTOPLASM; INDUSTRIAL WASTE; INHIBITION; INHIBITOR; SULFATE-REDUCING BACTERIUM; TOXICITY;

AMPLICON; ARTICLE; COMPETITIVE INHIBITION; DESULFOVIBRIO; DESULFOVIBRIO ALASKENSIS; DESULFOVIBRIONALES; DNA SEQUENCE; ENRICHMENT CULTURE; GROWTH INHIBITION; HYDROLYSIS; IC50; MICROBIAL COMMUNITY; MICROBIAL GROWTH; NONHUMAN; ORGANISMS BY PHYLOGENETIC POSITION; PH; PHENOTYPIC VARIATION; PHOSPHATE METABOLISM; SULFATE REDUCER; AEROBIC METABOLISM; BACTERIUM; DRUG EFFECTS; FERMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PHYLOGENY;

EUKARYOTA;

AEROBIOSIS; ANIONS; BACTERIA; CHLORIDES; DESULFOVIBRIO; FERMENTATION; FLUORIDES; IONS; MUTATION; NITRITES; OXIDATION-REDUCTION; OXYGEN; PHOSPHATES; PHYLOGENY; SULFATES; SULFIDES;

EID: 84925002457     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es505843z     Document Type: Article

References (56)

1. WHO. Hydrogen Sulfide. In WHO Regional Publications, European Series: Denmark, 2000; pp 1-7.
2. Gieg, L. M.; Jack, T. R.; Foght, J. M. Biological souring and mitigation in oil reservoirs Appl. Microbiol. Biotechnol. 2011, 92 (2) 263-282
3. Postgate, J. R. Competitive and noncompetitive inhibitors of bacterial sulphate reduction J. Gen. Microbiol. 1952, 6 (1-2) 128-142
4. Greene, E. A.; Brunelle, V.; Jenneman, G. E.; Voordouw, G. Synergistic inhibition of microbial sulfide production by combinations of the metabolic inhibitor nitrite and biocides Appl. Environ. Microbiol. 2006, 72 (12) 7897-901
5. Fink, J. K. Petroleum Engineers Guide to Oil Field Chemicals and Fluids. Petroleum Engineers Guide to Oil Field Chemicals and Fluids, 2012, 1-785.
6. Youssef, N.; Elshahed, M. S.; McInerney, M. J. Microbial processes in oil fields: Culprits, problems, and opportunities Adv. Appl. Microbiol. 2008, 66, 141-251
7. Hubert, C., Microbial ecology of oil reservoir souring and its control by nitrate injection. In Handbook of Hydrocarbon and Lipid Microbiology; Springer: New York, 2010; pp 2753-2766.
8. Greene, E. A.; Hubert, C.; Nemati, M.; Jenneman, G. E.; Voordouw, G. Nitrite reductase activity of sulphate-reducing bacteria prevents their inhibition by nitrate-reducing, sulphide-oxidizing bacteria Environ. Microbiol. 2003, 5 (7) 607-617
9. Sorensen, J.; Tiedje, J. M.; Firestone, R. B. Inhibition by sulfide of nitric and nitrous oxide reduction by denitrifying Pseudomonas fluorescens Appl. Environ. Microbiol. 1980, 39 (1) 105-8
10. Zhou, J.; He, Q.; Hemme, C. L.; Mukhopadhyay, A.; Hillesland, K.; Zhou, A.; He, Z.; Van Nostrand, J. D.; Hazen, T. C.; Stahl, D. A.; Wall, J. D.; Arkin, A. P. How sulphate-reducing microorganisms cope with stress: lessons from systems biology Nat. Rev. Microbiol. 2011, 9 (6) 452-466
11. Carlson, H. K.; Kuehl, J. V.; Hazra, A. B.; Justice, N. B.; Stoeva, M. K.; Sczesnak, A.; Mullan, M. R.; Iavarone, A. T.; Engelbrektson, A.; Price, M. N.; Deutschbauer, A. M.; Arkin, A. P.; Coates, J. D. Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per)chlorate and nitrate ISME J. 2014, 10.1038/ismej.2014.216
12. Engelbrektson, A.; Hubbard, C. G.; Tom, L. M.; Boussina, A.; Jin, Y. T.; Wong, H.; Piceno, Y. M.; Carlson, H. K.; Conrad, M. E.; Anderson, G.; Coates, J. D. Inhibition of microbial sulfate reduction in a flow-through column system by (per)chlorate treatment Front. Microbiol. 2014, 5, 315
13. 2S coupled to (per)chlorate reduction Environ. Microbiol. Rep. 2014, 6 (6) 558-564
14. Hanna, E.; MacRae, I. J.; Medina, D. C.; Fisher, A. J.; Segel, I. H. ATP sulfurylase from the hyperthermophilic chemolithotroph Aquifex aeolicus Arch. Biochem. Biophys. 2002, 406 (2) 275-288
15. Renosto, F.; Patel, H. C.; Martin, R. L.; Thomassian, C.; Zimmerman, G.; Segel, I. H. Atp sulfurylase from higher plants: Kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach Leaf Arch. Biochem. Biophys. 1993, 307 (2) 272-285
16. Hanna, E.; Ng, K. F.; MacRae, I. J.; Bley, C. J.; Fisher, A. J.; Segel, I. H. Kinetic and stability properties of Penicillium chrysogenum ATP sulfurylase missing the C-terminal regulatory domain J. Biol. Chem. 2004, 279 (6) 4415-4424
17. Peck, H. D. The ATP-dependent reduction of sulfate with hydrogen in extracts of Desulfovibrio desulfuricans Proc. Natl. Acad. Sci. U. S. A. 1959, 45 (5) 701-708
18. Peck, H. D. The role of adenosine-5′-phosphosulfate in the reduction of sulfate to sulfite by Desulfovibrio desulfuricans J. Biol. Chem. 1962, 237, 198-203
19. Cypionka, H. Characterization of sulfate transport in Desulfovibrio desulfuricans Arch. Microbiol. 1989, 152 (3) 237-243
20. Taylor, B. F.; Oremland, R. S. Depletion of adenosine-triphosphate in Desulfovibrio by oxyanions of Group-VI elements Curr. Microbiol. 1979, 3 (2) 101-103
21. Oremland, R. S.; Taylor, B. F. Sulfate reduction and methanogenesis in marine sediments Geochim. Cosmochim. Acta 1978, 42 (2) 209-214
22. Satishchandran, C.; Myers, C. B.; Markham, G. D. Adenosine-5′- O -(2-fluorodiphosphate) (ADP-beta-F), an analog of adenosine-5′-phosphosulfate Bioorg. Chem. 1992, 20 (2) 107-114
23. Price, M. N.; Deutschbauer, A. M.; Skerker, J. M.; Wetmore, K. M.; Ruths, T.; Mar, J. S.; Kuehl, J. V.; Shao, W.; Arkin, A. P. Indirect and suboptimal control of gene expression is widespread in bacteria Mol. Syst. Biol. 2013, 9, 660
24. Mukhopadhyay, A.; He, Z.; Alm, E. J.; Arkin, A. P.; Baidoo, E. E.; Borglin, S. C.; Chen, W.; Hazen, T. C.; He, Q.; Holman, H. Y.; Huang, K.; Huang, R.; Joyner, D. C.; Katz, N.; Keller, M.; Oeller, P.; Redding, A.; Sun, J.; Wall, J.; Wei, J.; Yang, Z.; Yen, H. C.; Zhou, J.; Keasling, J. D. Salt stress in Desulfovibrio vulgaris Hildenborough: an integrated genomics approach J. Bacteriol. 2006, 188 (11) 4068-78
25. European Committee for Antimicrobial Susceptibility Testing of the European Society of Clinical, M.; Infectious, D., EUCASTDefinitive Document E.Def 1.2, May 2000: Terminology relating to methodsfor the determination of susceptibility of bacteria to antimicrobialagents. Clin. Microbiol. Infect. 2000, 6 (9), 503-508.
26. Kozich, J. J.; Westcott, S. L.; Baxter, N. T.; Highlander, S. K.; Schloss, P. D. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform Appl. Environ. Microbiol. 2013, 79 (17) 5112-5120
27. Fadrosh, D. W.; Ma, B.; Gajer, P.; Sengamalay, N.; Ott, S.; Brotman, R. M.; Ravel, J. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform Microbiome 2014, 2 (1) 6
28. Zhang, J.; Kobert, K.; Flouri, T.; Stamatakis, A. A fast and accurate illumina paired-end reAd merge RPEAR. Bioinformatics 2014, 30 (5), 614-620.
29. Caporaso, J. G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F. D.; Costello, E. K.; Fierer, N.; Pena, A. G.; Goodrich, J. K.; Gordon, J. I.; Huttley, G. A.; Kelley, S. T.; Knights, D.; Koenig, J. E.; Ley, R. E.; Lozupone, C. A.; McDonald, D.; Muegge, B. D.; Pirrung, M.; Reeder, J.; Sevinsky, J. R.; Turnbaugh, P. J.; Walters, W. A.; Widmann, J.; Yatsunenko, T.; Zaneveld, J.; Knight, R. QIIME allows analysis of high-throughput community sequencing data Nat. Methods 2010, 7 (5) 335-336
30. Bourne, D. G.; Muirhead, A.; Sato, Y. Changes in sulfate-reducing bacterial populations during the onset of black band disease ISME J. 2011, 5 (3) 559-564
31. Leloup, J.; Loy, A.; Knab, N. J.; Borowski, C.; Wagner, M.; Jorgensen, B. B. Diversity and abundance of sulfate-reducing microorganisms in the sulfate and methane zones of a marine sediment, Black Sea Environ. Microbiol. 2007, 9 (1) 131-142
32. Tor, J. M.; Amend, J. P.; Lovley, D. R. Metabolism of organic compounds in anaerobic, hydrothermal sulphate-reducing marine sediments Environ. Microbiol. 2003, 5 (7) 583-591
33. Tucker, M. D.; Barton, L. L.; Thomson, B. M. Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilized in polyacrylamide gels J. Ind. Microbiol. Biot. 1998, 20 (1) 13-19
34. Zehr, J. P.; Oremland, R. S. Reduction of selenate to selenide by sulfate-respiring bacteria: experiments with cell suspensions and estuarine sediments Appl. Environ. Microbiol. 1987, 53 (6) 1365-1369
35. Achenbach, L. A.; Michaelidou, U.; Bruce, R. A.; Fryman, J.; Coates, J. D. Dechloromonas agitata gen. nov., sp. nov. and Dechlorosoma suillum gen. nov., sp. nov., two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position Int. J. Syst. Evol. Microbiol. 2001, 51 (Pt 2) 527-533
36. Lehar, J.; Krueger, A. S.; Avery, W.; Heilbut, A. M.; Johansen, L. M.; Price, E. R.; Rickles, R. J.; Short, G. F., 3rd; Staunton, J. E.; Jin, X.; Lee, M. S.; Zimmermann, G. R.; Borisy, A. A. Synergistic drug combinations tend to improve therapeutically relevant selectivity Nat. Biotechnol. 2009, 27 (7) 659-666
37. Kuehl, J. V.; Price, M. N.; Ray, J.; Wetmore, K. M.; Esquivel, Z.; Kazakov, A. E.; Nguyen, M.; Kuehn, R.; Davis, R. W.; Hazen, T. C.; Arkin, A. P.; Deutschbauer, A. Functional genomics with a comprehensive library of transposon mutants for the sulfate-reducing bacterium Desulfovibrio alaskensis G20 mBio 2014, 5 (3) e01041-e01114
38. Korte, H. L.; Fels, S. R.; Christensen, G. A.; Price, M. N.; Kuehl, J. V.; Zane, G. M.; Deutschbauer, A. M.; Arkin, A. P.; Wall, J. D. Genetic basis for nitrate resistance in Desulfovibrio strains Front. Microbiol. 2014, 5, 153
39. Li, X.; Krumholz, L. R. Regulation of arsenate resistance in Desulfovibrio desulfuricans G20 by an arsRBCC operon and an arsC gene J. Bacteriol. 2007, 189 (10) 3705-3711
40. Wolfe, B. M.; Lui, S. M.; Cowan, J. A. Desulfoviridin, a multimeric-dissimilatory sulfite reductase from Desulfovibrio vulgaris (Hildenborough). Purification, characterization, kinetics and EPR studies Eur. J. Biochem. 1994, 223 (1) 79-89
41. Meyer, B.; Kuehl, J. V.; Price, M. N.; Ray, J.; Deutschbauer, A. M.; Arkin, A. P.; Stahl, D. A. The energy-conserving electron transfer system used by Desulfovibrio alaskensis strain G20 during pyruvate fermentation involves reduction of endogenously formed fumarate and cytoplasmic and membrane-bound complexes, Hdr-Flox and Rnf Environ. Microbiol. 2014, 16 (11) 3463-3486
42. Lie, T. J.; Godchaux, W.; Leadbetter, E. R. Sulfonates as terminal electron acceptors for growth of sulfite-reducing bacteria (Desulfitobacterium spp.) and sulfate-reducing bacteria: effects of inhibitors of sulfidogenesis Appl. Environ. Microbiol. 1999, 65 (10) 4611-4617
43. Yurkiw, M. A.; Voordouw, J.; Voordouw, G. Contribution of rubredoxin:oxygen oxidoreductases and hybrid cluster proteins of Desulfovibrio vulgaris Hildenborough to survival under oxygen and nitrite stress Environ. Microbiol. 2012, 14 (10) 2711-2725
44. Breaker, R. R. New insight on the response of bacteria to fluoride Caries Res. 2012, 46 (1) 78-81
45. Baker, J. L.; Sudarsan, N.; Weinberg, Z.; Roth, A.; Stockbridge, R. B.; Breaker, R. R. Widespread genetic switches and toxicity resistance proteins for fluoride Science 2012, 335 (6065) 233-235
46. Mota, C. S.; Valette, O.; Gonzalez, P. J.; Brondino, C. D.; Moura, J. J.; Moura, I.; Dolla, A.; Rivas, M. G. Effects of molybdate and tungstate on expression levels and biochemical characteristics of formate dehydrogenases produced by Desulfovibrio alaskensis NCIMB 13491 J. Bacteriol. 2011, 193 (12) 2917-2923
47. Heijerick, D. G.; Regoli, L.; Carey, S. The toxicity of molybdate to freshwater and marine organisms. II. Effects assessment of molybdate in the aquatic environment under REACH Sci. Total Environ. 2012, 435-436, 179-187
48. Treibs, A. On the occurrence of chlorophyll-derivatives in an oil-slate in the upper trias Liebigs Ann. Chem. 1934, 509, 103-114
49. Hoorn, R. K. J.; Flikweert, J. P.; Staal, G. E. J. Purification and properties of enolase of human erythrocytes Int. J. Biochem. 1974, 5 (11-12) 845-852
50. Qin, R.; Chai, G. Q.; Brewer, J. M.; Lovelace, L. L.; Lebioda, L. Fluoride inhibition of enolase: Crystal structure and thermodynamics Biochemistry-U.S. 2006, 45 (3) 793-800
51. Ngala, V. T.; Page, C. L.; Page, M. M. Corrosion inhibitor systems for remedial treatment of reinforced concrete. Part 2: Sodium monofluorophosphate Corros. Sci. 2003, 45 (7) 1523-1537
52. Soylev, T. A.; Richardson, M. G. Corrosion inhibitors for steel in concrete: State-of-the-art report Constr. Build. Mater. 2008, 22 (4) 609-622
53. Setnikar, I.; Arigoni, R. Chemical stability and mode of gastrointestinal absorption of sodium monofluorophosphate Arzneimittelforschung 1988, 38 (1) 45-49
54. Fernley, H. N.; Walker, P. G. Studies on alkaline phosphatase. Inhibition by phosphate derivatives and the substrate specificity Biochem. J. 1967, 104 (3) 1011-1018
55. Tietz, A.; Ochoa, S. Fluorokinase and pyruvic kinase Arch. Biochem. Biophys. 1958, 78 (2) 477-493
56. Rowley, H. H.; Stuckey, J. E. Preparation and properties of calcium monofluorophosphate dihydrate J. Am. Chem. Soc. 1956, 78 (17) 4262-4263