1887

Abstract

Microbial sulfate reduction (SR) by sulfate-reducing micro-organisms (SRM) is a primary environmental mechanism of anaerobic organic matter mineralization, and as such influences carbon and sulfur cycling in many natural and engineered environments. In industrial systems, SR results in the generation of hydrogen sulfide, a toxic, corrosive gas with adverse human health effects and significant economic and environmental consequences. Therefore, there has been considerable interest in developing strategies for mitigating hydrogen sulfide production, and several specific inhibitors of SRM have been identified and characterized. Specific inhibitors are compounds that disrupt the metabolism of one group of organisms, with little or no effect on the rest of the community. Putative specific inhibitors of SRM have been used to control sulfidogenesis in industrial and engineered systems. Despite the value of these inhibitors, mechanistic and quantitative studies into the molecular mechanisms of their inhibition have been sparse and unsystematic. The insight garnered by such studies is essential if we are to have a more complete understanding of SR, including the past and current selective pressures acting upon it. Furthermore, the ability to reliably control sulfidogenesis – and potentially assimilatory sulfate pathways – relies on a thorough molecular understanding of inhibition. The scope of this review is to summarize the current state of the field: how we measure and understand inhibition, the targets of specific SR inhibitors and how SRM acclimatize and/or adapt to these stressors.

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2018-12-17
2019-10-18
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References

  1. Bowles MW, Mogollón JM, Kasten S, Zabel M, Hinrichs KU. Global rates of marine sulfate reduction and implications for sub-sea-floor metabolic activities. Science 2014;344:889–891 [CrossRef][PubMed]
    [Google Scholar]
  2. Muyzer G, Stams AJM. The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 2008;6:441–454 [CrossRef]
    [Google Scholar]
  3. Barton LL, Fauque GD. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. In Adv Appl Microbiol Elsevier Inc.; 2009; pp.41–98
    [Google Scholar]
  4. Akagi JM, Barton LL, Chen L, Cypionka H, Devereux R et al. Sulfate-Reducing Bacteria US: Springer; 1995
    [Google Scholar]
  5. Rabus R, Venceslau SS, Wöhlbrand L, Voordouw G, Wall JD et al. A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. In Poole RK. (editor) Advances in Microbial Physiology Oxford: Academic Press; 2015; pp.55–321
    [Google Scholar]
  6. Cypionka H. Characterization of sulfate transport in Desulfovibrio desulfuricans. Arch Microbiol 1989;152:237–243 [CrossRef][PubMed]
    [Google Scholar]
  7. Warthmann R, Cypionka H. Sulfate transport in Desulfobulbus propionicus and Desulfococcus multivorans. Arch Microbiol 1990;154:144–149 [CrossRef]
    [Google Scholar]
  8. Santos AA, Venceslau SS, Grein F, Leavitt WD, Dahl C et al. A protein trisulfide couples dissimilatory sulfate reduction to energy conservation. Science 2015;350:1541–1545 [CrossRef][PubMed]
    [Google Scholar]
  9. Grein F, Ramos AR, Venceslau SS, Pereira IA. Unifying concepts in anaerobic respiration: insights from dissimilatory sulfur metabolism. Biochim Biophys Acta 2013;1827:145–160 [CrossRef][PubMed]
    [Google Scholar]
  10. Carlson HK, Stoeva MK, Justice NB, Sczesnak A, Mullan MR et al. Monofluorophosphate Is a selective inhibitor of respiratory sulfate-reducing microorganisms. Environ Sci Technol 2015;49:3727–3736 [CrossRef]
    [Google Scholar]
  11. Oremland RS, Capone DG. Use of "specific" inhibitors in biogeochemistry and microbial ecology. Adv Microb Ecol 1988;10:285–383
    [Google Scholar]
  12. Liu H, Wang J, Wang A, Chen J. Chemical inhibitors of methanogenesis and putative applications. Appl Microbiol Biotechnol 2011;89:1333–1340 [CrossRef][PubMed]
    [Google Scholar]
  13. Postgate J. Competitive inhibition of sulphate reduction by selenate. Nature 1949;164:670–671 [CrossRef]
    [Google Scholar]
  14. Postgate JR. Competitive and noncompetitive inhibitors of bacterial sulphate reduction. J Gen Microbiol 1952;6:128–142 [CrossRef][PubMed]
    [Google Scholar]
  15. Ortega Morente E, Fernández-Fuentes MA, Grande Burgos MJ, Abriouel H, Pérez Pulido R et al. Biocide tolerance in bacteria. Int J Food Microbiol 2013;162:13–25 [CrossRef]
    [Google Scholar]
  16. Blair JM, Webber MA, Baylay AJ, Ogbolu DO, Piddock LJ. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol 2015;13:42–51 [CrossRef][PubMed]
    [Google Scholar]
  17. Korte HL, Fels SR, Christensen GA, Price MN, Kuehl JV et al. Genetic basis for nitrate resistance in Desulfovibrio strains. Front Microbiol 2014;5:153 [CrossRef][PubMed]
    [Google Scholar]
  18. Gieg LM, Jack TR, Foght JM. Biological souring and mitigation in oil reservoirs. Appl Microbiol Biotechnol 2011;92:263–282 [CrossRef]
    [Google Scholar]
  19. Mohanakrishnan J, Kofoed MVW, Barr J, Yuan Z, Schramm A et al. Dynamic microbial response of sulfidogenic wastewater biofilm to nitrate. Appl Microbiol Biotechnol 2011;91:1647–1657 [CrossRef]
    [Google Scholar]
  20. Voordouw G, Grigoryan AA, Lambo A, Lin S, Park HS et al. Sulfide remediation by pulsed injection of nitrate into a low temperature Canadian heavy oil reservoir. Environ Sci Technol 2009;43:9512–9518 [CrossRef][PubMed]
    [Google Scholar]
  21. Engelbrektson A, Hubbard CG, Tom LM, Boussina A, Jin YT et al. Inhibition of microbial sulfate reduction in a flow-through column system by (per)chlorate treatment. Front Microbiol 2014;5:315 [CrossRef]
    [Google Scholar]
  22. Gregoire P, Engelbrektson A, Hubbard CG, Metlagel Z, Csencsits R et al. Control of sulfidogenesis through bio-oxidation of H2S coupled to (per)chlorate reduction. Environ Microbiol Rep 2014;6:558–564 [CrossRef][PubMed]
    [Google Scholar]
  23. Cheng Y, Hubbard CG, Li L, Bouskill N, Molins S et al. Reactive transport model of sulfur cycling as impacted by perchlorate and nitrate treatments. Environ Sci Technol 2016;50:7010–7018 [CrossRef][PubMed]
    [Google Scholar]
  24. Engelbrektson AL, Cheng Y, Hubbard CG, Jin YT, Arora B et al. Attenuating sulfidogenesis in a soured continuous flow column system with perchlorate treatment. Front Microbiol 2018;9:1575 [CrossRef][PubMed]
    [Google Scholar]
  25. Stoeva MK, Nalula G, Garcia N, Yiwei C, Engelbrektson A et al. Resistance and resilience of sulfidogenic communities in the face of the competitive inhibitor perchlorate. (In prep)
  26. Saleh AM, MacPherson R, Miller JDA. The effect of inhibitors on sulphate reducing bacteria: a compilation. J Appl Bacteriol 1964;27:281–293 [CrossRef]
    [Google Scholar]
  27. Taylor BF, Oremland RS. Depletion of adenosine triphosphate in desulfovibrio by oxyanions of group VI elements. Curr Microbiol 1979;3:101–103 [CrossRef]
    [Google Scholar]
  28. Carlson HK, Kuehl JV, Hazra AB, Justice NB, Stoeva MK et al. Mechanisms of direct inhibition of the respiratory sulfate-reduction pathway by (per)chlorate and nitrate. ISME J 2015;9:1295–1305 [CrossRef][PubMed]
    [Google Scholar]
  29. Carlson HK, Mullan MR, Mosqueda LA, Chen S, Arkin MR et al. High-throughput screening to identify potent and specific inhibitors of microbial sulfate reduction. Environ Sci Technol 2017;51:7278–7285 [CrossRef][PubMed]
    [Google Scholar]
  30. He Q, Huang KH, He Z, Alm EJ, Fields MW et al. Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl Environ Microbiol 2006;72:4370–4381 [CrossRef][PubMed]
    [Google Scholar]
  31. Redding AM, Mukhopadhyay A, Joyner DC, Hazen TC, Keasling JD. Study of nitrate stress in Desulfovibrio vulgaris Hildenborough using iTRAQ proteomics. Brief Funct Genomic Proteomic 2006;5:133–143 [CrossRef][PubMed]
    [Google Scholar]
  32. Haveman SA, Greene EA, Stilwell CP, Voordouw JK, Voordouw G. Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris hildenborough by nitrite. J Bacteriol 2004;186:7944–7950 [CrossRef][PubMed]
    [Google Scholar]
  33. He Q, He Z, Joyner DC, Joachimiak M, Price MN et al. Impact of elevated nitrate on sulfate-reducing bacteria: a comparative study of Desulfovibrio vulgaris. ISME J 2010;4:1386–1397 [CrossRef][PubMed]
    [Google Scholar]
  34. Nair RR, Silveira CM, Diniz MS, Almeida MG, Moura JJ et al. Changes in metabolic pathways of Desulfovibrio alaskensis G20 cells induced by molybdate excess. J Biol Inorg Chem 2015;20:311–322 [CrossRef][PubMed]
    [Google Scholar]
  35. Zhou J, He Q, Hemme CL, Mukhopadhyay A, Hillesland K et al. How sulphate-reducing microorganisms cope with stress: lessons from systems biology. Nat Rev Microbiol 2011;9:452–466 [CrossRef][PubMed]
    [Google Scholar]
  36. Price MN, Deutschbauer AM, Skerker JM, Wetmore KM, Ruths T et al. Indirect and suboptimal control of gene expression is widespread in bacteria. Mol Syst Biol 2013;9:660 [CrossRef]
    [Google Scholar]
  37. Skerker JM, Leon D, Price MN, Mar JS, Tarjan DR et al. Dissecting a complex chemical stress: chemogenomic profiling of plant hydrolysates. Mol Syst Biol 2013;9:674 [CrossRef]
    [Google Scholar]
  38. Cokol M, Chua HN, Tasan M, Mutlu B, Weinstein ZB et al. Systematic exploration of synergistic drug pairs. Mol Syst Biol 2011;7:544 [CrossRef]
    [Google Scholar]
  39. EUCAST Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. 2000
  40. Greene EA, Brunelle V, Jenneman GE, Voordouw G. Synergistic inhibition of microbial sulfide production by combinations of the metabolic inhibitor nitrite and biocides. Appl Environ Microbiol 2006;72:7897–7901 [CrossRef][PubMed]
    [Google Scholar]
  41. Lehár J, Krueger AS, Avery W, Heilbut AM, Johansen LM et al. Synergistic drug combinations tend to improve therapeutically relevant selectivity. Nat Biotechnol 2009;27:659–666 [CrossRef][PubMed]
    [Google Scholar]
  42. Aguilar-Barajas E, Díaz-Pérez C, Ramírez-Díaz MI, Riveros-Rosas H, Cervantes C. Bacterial transport of sulfate, molybdate, and related oxyanions. Biometals 2011;24:687–707 [CrossRef][PubMed]
    [Google Scholar]
  43. Takahashi H. Regulation of Sulfate Transport and Assimilation in Plants, 1st ed. Elsevier Inc; 2010
    [Google Scholar]
  44. Alper SL, Sharma AK. The SLC26 gene family of anion transporters and channels. Mol Aspects Med 2013;34:494–515 [CrossRef][PubMed]
    [Google Scholar]
  45. Shlykov MA, Zheng WH, Chen JS, Saier MH. Bioinformatic characterization of the 4-Toluene Sulfonate Uptake Permease (TSUP) family of transmembrane proteins. Biochim Biophys Acta 2012;1818:703–717 [CrossRef][PubMed]
    [Google Scholar]
  46. Piłsyk S, Paszewski A. Sulfate permeasesphylogenetic diversity of sulfate transport. Acta Biochim Pol 2009;56:375–384[PubMed]
    [Google Scholar]
  47. Stahlmann J, Warthmann R, Cypionka H. Na+-dependent accumulation of sulfate and thiosulfate in marine sulfate-reducing bacteria. Arch Microbiol 1991;155:554–558 [CrossRef]
    [Google Scholar]
  48. Kreke B, Cypionka H. Role of sodium ions for sulfate transport and energy metabolism in Desulfovibrio salexigens. Arch Microbiol 1994;161:55–61 [CrossRef]
    [Google Scholar]
  49. Cypionka H. [1] Sulfate transport. Methods in Enzymologyvol. 243 Academic Press; 1994; pp.3–14
    [Google Scholar]
  50. Tarpgaard IH, Jørgensen BB, Kjeldsen KU, Røy H. The marine sulfate reducer Desulfobacterium autotrophicum HRM2 can switch between low and high apparent half-saturation constants for dissimilatory sulfate reduction. FEMS Microbiol Ecol 2017;93:1–11 [CrossRef][PubMed]
    [Google Scholar]
  51. Marietou A, Røy H, Jørgensen BB, Kjeldsen KU. Sulfate transporters in dissimilatory sulfate reducing microorganisms: a comparative genomics analysis. Front Microbiol 2018;9:1–21 [CrossRef][PubMed]
    [Google Scholar]
  52. Aguilar-Barajas E, Díaz-Pérez C, Ramírez-Díaz MI, Riveros-Rosas H, Cervantes C. Bacterial transport of sulfate, molybdate, and related oxyanions. Biometals 2011;24:687–707 [CrossRef][PubMed]
    [Google Scholar]
  53. Keller KL, Wall JD. Genetics and molecular biology of the electron flow for sulfate respiration in Desulfovibrio. Front Microbiol 2011;2:1–17 [CrossRef]
    [Google Scholar]
  54. Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK et al. MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 2010;38:D396–D400 [CrossRef][PubMed]
    [Google Scholar]
  55. Lo V, Shao W, Price M. Fitness browser. http://fit.genomics.lbl.gov/cgi-bin/myFrontPage.cgi [accessed December 9, 2018]
  56. Gisin J, Müller A, Pfänder Y, Leimkühler S, Narberhaus F et al. A Rhodobacter capsulatus member of a universal permease family imports molybdate and other oxyanions. J Bacteriol 2010;192:5943–5952 [CrossRef][PubMed]
    [Google Scholar]
  57. Hoffmann MC, Pfänder Y, Tintel M, Masepohl B. Bacterial pero permeases transport sulfate and related oxyanions. J Bacteriol 2017;199: [CrossRef][PubMed]
    [Google Scholar]
  58. Mansilla MC, de Mendoza D. The Bacillus subtilis cysP gene encodes a novel sulphate permease related to the inorganic phosphate transporter (Pit) family. Microbiology 2000;146:815–821 [CrossRef][PubMed]
    [Google Scholar]
  59. Rückert C, Koch DJ, Rey DA, Albersmeier A, Mormann S et al. Functional genomics and expression analysis of the Corynebacterium glutamicum fpr2-cysIXHDNYZ gene cluster involved in assimilatory sulphate reduction. BMC Genomics 2005;6:121–18 [CrossRef][PubMed]
    [Google Scholar]
  60. Zhang L, Jiang W, Nan J, Almqvist J, Huang Y. The Escherichia coli CysZ is a pH dependent sulfate transporter that can be inhibited by sulfite. Biochim Biophys Acta 2014;1838:1809–1816 [CrossRef][PubMed]
    [Google Scholar]
  61. Cherest H, Davidian JC, Thomas D, Benes V, Ansorge W et al. Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 1997;145:627–635[PubMed]
    [Google Scholar]
  62. Smith FW, Hawkesford MJ, Prosser IM, Clarkson DT. Isolation of a cDNA from Saccharomyces cerevisiae that encodes a high affinity sulphate transporter at the plasma membrane. Mol Gen Genet 1995;247:709–715 [CrossRef][PubMed]
    [Google Scholar]
  63. Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H et al. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 2002;29:475–486 [CrossRef][PubMed]
    [Google Scholar]
  64. El Kassis E, Cathala N, Rouached H, Fourcroy P, Berthomieu P et al. Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 2007;143:1231–1241 [CrossRef][PubMed]
    [Google Scholar]
  65. Parra F, Britton P, Castle C, Jones-Mortimer MC, Kornberg HL. Two separate genes involved in sulphate transport in Escherichia coli K12. J Gen Microbiol 1983;129:357–358 [CrossRef][PubMed]
    [Google Scholar]
  66. Bevers LE, Hagedoorn PL, Krijger GC, Hagen WR. Tungsten transport protein A (WtpA) in Pyrococcus furiosus: the first member of a new class of tungstate and molybdate transporters. J Bacteriol 2006;188:6498–6505 [CrossRef][PubMed]
    [Google Scholar]
  67. Otrelo-Cardoso AR, Nair RR, Correia MA, Rivas MG, Santos-Silva T. TupA: a tungstate binding protein in the periplasm of Desulfovibrio alaskensis G20. Int J Mol Sci 2014;15:11783–11798 [CrossRef][PubMed]
    [Google Scholar]
  68. Mota CS, Valette O, González PJ, Brondino CD, Moura JJ et al. Effects of molybdate and tungstate on expression levels and biochemical characteristics of formate dehydrogenases produced by Desulfovibrio alaskensis NCIMB 13491. J Bacteriol 2011;193:2917–2923 [CrossRef][PubMed]
    [Google Scholar]
  69. Kazakov AE, Rajeev L, Luning EG, Zane GM, Siddartha K et al. New family of tungstate-responsive transcriptional regulators in sulfate-reducing bacteria. J Bacteriol 2013;195:4466–4475 [CrossRef][PubMed]
    [Google Scholar]
  70. Korte HL, Saini A, Trotter VV, Butland GP, Arkin AP et al. Independence of nitrate and nitrite inhibition of Desulfovibrio vulgaris Hildenborough and use of nitrite as a substrate for growth. Environ Sci Technol 2015;49:924–931 [CrossRef][PubMed]
    [Google Scholar]
  71. Prioretti L, Gontero B, Hell R, Giordano M. Diversity and regulation of ATP sulfurylase in photosynthetic organisms. Front Plant Sci 2014;5:1–12 [CrossRef][PubMed]
    [Google Scholar]
  72. Parey K, Demmer U, Warkentin E, Wynen A, Ermler U et al. Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS One 2013;8: [CrossRef][PubMed]
    [Google Scholar]
  73. Gavel OY, Bursakov SA, Calvete JJ, George GN, Moura JJ et al. ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. Biochemistry 1998;37:16225–16232 [CrossRef][PubMed]
    [Google Scholar]
  74. Hanna E, Ng KF, MacRae IJ, Bley CJ, Fisher AJ et al. Kinetic and stability properties of Penicillium chrysogenum ATP sulfurylase missing the C-terminal regulatory domain. J Biol Chem 2004;279:4415–4424 [CrossRef][PubMed]
    [Google Scholar]
  75. Renosto F, Patel HC, Martin RL, Thomassian C, Zimmerman G et al. ATP sulfurylase from higher plants: kinetic and structural characterization of the chloroplast and cytosol enzymes from spinach leaf. Arch Biochem Biophys 1993;307:272–285 [CrossRef][PubMed]
    [Google Scholar]
  76. Newport PJ, Nedwell DB. The mechanisms of inhibition of Desulfovibrio and Desulfotomaculum. J Appl Bacteriol 1988;65:419–423
    [Google Scholar]
  77. Satishchandran C, Myers CB, Markham GD. Adenosine-5′-O-(2-fluorodiphosphate) (ADPβF), an analog of adenosine-5′-phosphosulfate. Bioorg Chem 1992;20:107–114 [CrossRef]
    [Google Scholar]
  78. Schiavon M, Pittarello M, Pilon-Smits EAH, Wirtz M, Hell R et al. Selenate and molybdate alter sulfate transport and assimilation in Brassica juncea L. Czern.: Implications for phytoremediation. Environ Exp Bot 2012;75:41–51 [CrossRef]
    [Google Scholar]
  79. Yu M, Martin RL, Jain S, Chen LJ, Segel IH. Rat liver ATP-sulfurylase: purification, kinetic characterization, and interaction with arsenate, selenate, phosphate, and other inorganic oxyanions. Arch Biochem Biophys 1989;269:156–174 [CrossRef][PubMed]
    [Google Scholar]
  80. Lyle S, Geller DH, Ng K, Stanczak J, Westley J et al. Kinetic mechanism of adenosine 5'-phosphosulphate kinase from rat chondrosarcoma. Biochem J 1994;301:355–359 [CrossRef][PubMed]
    [Google Scholar]
  81. Ullrich TC, Huber R. The complex structures of ATP sulfurylase with thiosulfate, ADP and chlorate reveal new insights in inhibitory effects and the catalytic cycle. J Mol Biol 2001;313:1117–1125 [CrossRef][PubMed]
    [Google Scholar]
  82. Mehta MG, Stoeva MK, Mehra A, Redford SA, Youngblut M et al. Adaptation of Desulfovibrio alaskensis G20 to perchlorate, a specific inhibitor of sulfate reduction. Submitted to Environmental Microbiology
  83. Lampreia J, Pereira AS, Moura JJ. Adenylylsulfate reductase from sulfate-reducing bacteria. Methods Enzymol 1994;243:241–260
    [Google Scholar]
  84. Senaratne RH, de Silva AD, Williams SJ, Mougous JD, Reader JR et al. 5'-Adenosinephosphosulphate reductase (CysH) protects Mycobacterium tuberculosis against free radicals during chronic infection phase in mice. Mol Microbiol 2006;59:1744–1753 [CrossRef][PubMed]
    [Google Scholar]
  85. Cosconati S, Hong JA, Novellino E, Carroll KS, Goodsell DS et al. Structure-based virtual screening and biological evaluation of Mycobacterium tuberculosis adenosine 5'-phosphosulfate reductase inhibitors. J Med Chem 2008;51:6627–6630 [CrossRef][PubMed]
    [Google Scholar]
  86. Hong JA, Bhave DP, Carroll KS. Identification of critical ligand binding determinants in Mycobacterium tuberculosis adenosine-5'-phosphosulfate reductase. J Med Chem 2009;52:5485–5495 [CrossRef][PubMed]
    [Google Scholar]
  87. Campanini B, Pieroni M, Raboni S, Bettati S, Benoni R et al. Inhibitors of the sulfur assimilation pathway in bacterial pathogens as enhancers of antibiotic therapy. Curr Med Chem 2015;22:187–213 [CrossRef][PubMed]
    [Google Scholar]
  88. Wolfe BM, Lui SM, Cowan JA. Desulfoviridin, a multimeric-dissimilatory sulfite reductase from Desulfovibrio vulgaris (Hildenborough). Purification, characterization, kinetics and EPR studies. Eur J Biochem 1994;223:79–89 [CrossRef][PubMed]
    [Google Scholar]
  89. Marietou A. Nitrate reduction in sulfate-reducing bacteria. FEMS Microbiol Lett 2016;363:fnw155 [CrossRef]
    [Google Scholar]
  90. Moura I, Bursakov S, Costa C, Moura JJG. Nitrate and nitrite utilization in sulfate-reducing bacteria. Anaerobe 1997;3:279–290 [CrossRef][PubMed]
    [Google Scholar]
  91. Cadby IT, Faulkner M, Cheneby J, Long J, van Helden J et al. Coordinated response of the Desulfovibrio desulfuricans 27774 transcriptome to nitrate, nitrite and nitric oxide. Sci Rep 2017;7:1–16 [CrossRef]
    [Google Scholar]
  92. Plugge CM, Zhang W, Scholten JC, Stams AJ. Metabolic flexibility of sulfate-reducing bacteria. Front Microbiol 2011;2:81 [CrossRef][PubMed]
    [Google Scholar]
  93. Christensen GA, Zane GM, Kazakov AE, Li X, Rodionov DA et al. Rex (encoded by DVU_0916) in Desulfovibrio vulgaris Hildenborough is a repressor of sulfate adenylyl transferase and is regulated by NADH. J Bacteriol 2015;197:29–39 [CrossRef][PubMed]
    [Google Scholar]
  94. Kuehl JV, Price MN, Ray J, Wetmore KM, Esquivel Z et al. Functional genomics with a comprehensive library of transposon mutants for the sulfate-reducing bacterium Desulfovibrio alaskensis G20. MBio 2014;5:1–13 [CrossRef][PubMed]
    [Google Scholar]
  95. Zane GM, De Leon KB. Novel mode of molybdate inhibition of Desulfovibrio vulgaris Hildenborough. In Poster Presented at ASM 2017 2017
    [Google Scholar]
  96. Wiatr CL, Fedyniak OX. Development of an obligate anaerobe specific biocide. J Ind Microbiol 1991;7:7–13 [CrossRef]
    [Google Scholar]
  97. Edwards DI. Nitroimidazole drugs-action and resistance mechanisms. I. Mechanism of action. J Antimicrob Chemother 1993;31:9–20 [CrossRef][PubMed]
    [Google Scholar]
  98. Cline J. Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 1969;14:454–458 [CrossRef]
    [Google Scholar]
  99. Zolotarev AS, Unnikrishnan M, Shmukler BE, Clark JS, Vandorpe DH et al. Increased sulfate uptake by E. coli overexpressing the SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis. Comp Biochem Physiol-A Mol Integr Physiol 2008;149:255–266 [CrossRef]
    [Google Scholar]
  100. Barberon M, Berthomieu P, Clairotte M, Shibagaki N, Davidian J-C et al. Unequal functional redundancy between the two Arabidopsis thaliana high-affinity sulphate transporters SULTR1;1 and SULTR1;2. New Phytol 2008;180:608–619 [CrossRef]
    [Google Scholar]
  101. Fitzpatrick KL, Tyerman SD, Kaiser BN. Molybdate transport through the plant sulfate transporter SHST1. FEBS Lett 2008;582:1508–1513 [CrossRef]
    [Google Scholar]
  102. Hanna E, MacRae IJ, Medina DC, Fisher AJ, Segel IH. ATP sulfurylase from the hyperthermophilic chemolithotroph Aquifex aeolicus. Arch Biochem Biophys 2002;406:275–288 [CrossRef]
    [Google Scholar]
  103. Farley JR, Nakayama G, Cryns D, Segel IH. Adenosine triphosphate sulfurylase from Penicillium chrysogenum: equilibrium binding, substrate hydrolysis, and isotope exchange studies. Arch Biochem Biophys 1978;185:376–390 [CrossRef]
    [Google Scholar]
  104. Seubert PA, Renosto F, Knudson P, Segel IH. Adenosinetriphosphate sulfurylase from Penicillium chrysogenum: steady-state kinetics of the forward and reverse reactions, alternative substrate kinetics, and equilibrium binding studies. Arch Biochem Biophys 1985;240:509–523 [CrossRef]
    [Google Scholar]
  105. Foster BA, Thomas SM, Mahr JA, Renosto F, Patel HC et al. Cloning and sequencing of ATP sulfurylase from Penicillium chrysogenum. J Biol Chem 1994;269:19777–19786
    [Google Scholar]
  106. Seubert PA, Hoang L, Renosto F, Segel IH. ATP sulfurylase from Penicillium chrysogenum: measurements of the true specific activity of an enzyme subject to potent product inhibition and a reassessment of the kinetic mechanism. Arch Biochem Biophys 1983;225:679–691[PubMed]
    [Google Scholar]
  107. Ravilious GE, Herrmann J, Goo Lee S, Westfall CS, Jez JM. Kinetic mechanism of the dimeric ATP sulfurylase from plants. Biosci Rep 2013;33:585–591 [CrossRef][PubMed]
    [Google Scholar]
  108. Osslund T, Chandler C, Segel IH. ATP sulfurylase from higher plants. Plant Physiol 1982;70:39–45
    [Google Scholar]
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