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ATP sulfurylase activity of sulfate-reducing bacteria from various ecotopes


Sulfate-reducing bacteria (SRB) are widespread in various ecotopes despite their growth and enzymatic features not compared. In this study, the enzymatic parameters of ATP sulfurylase in cell-free extracts of sulfate-reducing bacteria isolated from various ecotopes such as soils, corrosion products and human large intestine were determined. Comparative analysis of both enzyme characteristics and growth parameters were carried out and similar research has not been reported yet. The initial and maximum rates of enzymatic reaction catalyzed by ATP sulfurylase were significantly different (p < 0.05) in the bacterial strains isolated from various environmental ecotopes. The specific activity of this enzyme in sulfate-reducing bacteria was determined for corrosive and intestinal strains 0.98–1.56 and 0.98–2.26 U × mg−1 protein, respectively. The Michaelis constants were 1.55–2.29 mM for corrosive and 2.93–3.13 mM for intestinal strains and the affinity range were demonstrated. Based on cluster analysis, the parameters of physiological and biochemical characteristics of sulfate-reducing bacteria from different ecotopes are divided into 3 clusters corresponding to the location of their isolation (soils, heating systems and human intestine). Understanding the enzymatic parameters of the initial stages of sulfate consumption in the process of dissimilatory sulfate reduction will allow the development of effective methods for controlling the production of toxic metabolites, including hydrogen sulfide.

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  1. Akagi JM (1981) Dissimilatory sulfate reduction, mechanistic aspects. Biology of Inorganic Nitrogen and Sulfur. Springer-Verlag, New-York, pp 178–187

  2. Asaulenko LH, Abdulina DR, Purish LM (2010) Taxonomic position of certain representatives of sulphate-reducing corrosive microbial community. Mikrobiol Zhurn 72(4):3–10

  3. Bailey NTJ (1995) Statistical methods in biology. Cambridge University Press, Cambridge, UK

  4. Barton LL, Hamilton WA (2010) Sulphate-Reducing Bacteria. Cambridge University Press, Environmental and Engineered Systems, p 553

  5. Černý M, Vítězová M, Vítěz T, Bartoš M, Kushkevych I (2018) Variation in the distribution of hydrogen producers from the clostridiales order in biogas reactors depending on different input substrates. Energies 11(12):3270

  6. Coutinho CMLM, Coutinho-Silva R, Zinkevich V, Pearce CB, Ojcius DM, Beech I (2017) Sulphate-reducing bacteria from ulcerative colitis patients induce apoptosis of gastrointestinal epithelial cells. Microb Pathog 112:126–134

  7. Dowd JE, Riggs DS (1965) A comparison of estimates of Michaelis-Menten kinetic constants from various linear transformations. J Biol Chem 240(2):863–869

  8. Gavel OY, Bursakov SA, Calvete JJ (1998) ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing Cobalt and Zinc. Biochemistry 37:16225–16232

  9. Herrmann JI, Ravilious GE, McKinney SE (2014) Structure and mechanism of soybean ATP sulfurylase and the committed step in plant sulfur assimilation. J Biol Chem 289(15):10919–10929

  10. Itoh T, Okabe S, Satoh H (2002) Successional development of sulfate-reducing bacterial populations and their activities in a wastewater biofilm growing under microaerophilic conditions. Appl Environ Microbiol 68(3):1392–1402

  11. Iutynska GA., Purish LM, Abdulina DR (2014) Corrosive-relevant sulfidogenic microbial communities of man-caused ecotopes. Lambert Academic Publishing, 173 p

  12. Keleti T (1988) Basic enzyme kinetics. Akademiai Kiado, 422 p

  13. Kováč J, Kushkevych I (2017) New modification of cultivation medium for isolation and growth of intestinal sulfate-reducing bacteria. In: Proceeding of international PhD students conference MendelNet, pp 702–707

  14. Kováč J, Vítězová M, Kushkevych I (2018) Metabolic activity of sulfate-reducing bacteria from rodents with colitis. Open Med 13:344–349

  15. Kramer M, Cypionka H (1989) Sulfate formation via ATP sulfyrylase in thiosulfate- and sulfite-disproportionating bacteria. Arch Microbiol 151:232–237

  16. Kushkevych IV (2015a) Activity and kinetic properties of phosphotransacetylase from intestinal sulfate-reducing bacteria. Acta Biochemica Polonica 62:1037–1108

  17. Kushkevych IV (2015b) Kinetic properties of pyruvate ferredoxin oxidoreductase of intestinal sulfate-reducing bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Polish J Microbiol 64:107–114

  18. Kushkevych I, Kollar P, Suchy P, Parak K, Pauk K, Imramovsky A (2015a) Activity of selected salicylamides against intestinal sulfate-reducing bacteria. Neuroendocrinol Lett 36:106–113

  19. Kushkevych I, Fafula R, Parak T, Bartos M (2015b) Activity of Na+/K+-activated Mg2+-dependent ATP hydrolase in the cell-free extracts of the sulfate-reducing bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Acta Vet Brno 84:3–12

  20. Kushkevych I, Kollar P, Ferreira AL, Palma D (2016) Antimicrobial effect of salicylamide derivatives against intestinal sulfate-reducing bacteria. J Appl Biomed 14:125–130

  21. Kushkevych I, Vítězová M, Fedrová M, Vochyanová Z, Paráková L, Hošek J (2017a) Kinetic properties of growth of intestinal sulphate-reducing bacteria isolated from healthy mice and mice with ulcerative colitis. Acta Vet Brno 86:405–411

  22. Kushkevych I, Vítězová M, Vítěz T, Bartoš M (2017b) Production of biogas: relationship between methanogenic and sulfate-reducing microorganisms. Open Life Sci 12:82–91

  23. Kushkevych I, Dordević D, Vítězová M, Kollár P (2018a) Cross-correlation analysis of the Desulfovibrio growth parameters of intestinal species isolated from people with colitis. Biologia 73:1137–1143

  24. Kushkevych I, Vítězová M, Vítěz T, Kováč J, Kaucká P, Jesionek W, Bartos M, Barton L (2018b) A new combination of substrates: biogas production and diversity of the methanogenic microorganisms. Open Life Sci 13:119–128

  25. Kushkevych I, Kos J, Kollar P, Kralova K, Jampilek J (2018c) Activity of ring-substituted 8-hydroxyquinoline-2-carboxanilides against intestinal sulfate-reducing bacteria Desulfovibrio piger. Med Chem Res 27:278–284

  26. Kushkevych I, Kováč J, Vítězová M, Vítěz T, Bartoš M (2018d) The diversity of sulfate-reducing bacteria in the seven bioreactors. Arch Microbiol 200:945–950

  27. Kushkevych I, Vítězová M, Kos J, Kollár P, Jampílek J (2018e) Effect of selected 8-hydroxyquinoline-2-carboxanilides on viability and sulfate metabolism of Desulfovibrio piger. J App Biomed 16:241–246

  28. Kushkevych I, Dordević D, Kollár P (2018f) Analysis of physiological parameters of Desulfovibrio strains from individuals with colitis. Open Life Sci 13(1):481–488

  29. Kushkevych I, Dordević D, Vítězová M (2019a) Analysis of pH dose-dependent growth of sulfate-reducing bacteria. Open Med 14(1):66–74

  30. Kushkevych I, Dordević D, Vítězová M (2019b) Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7. Arch Microbiol 201(3):389–397

  31. Linder T (2017) ATP Sulfurylase is Essential for the utilization of sulfamate as a sulfur source in the yeast Komagataella pastoris (syn. Pichia pastoris). Curr Microbiol 74(9):1021–1025

  32. Mander GJ, Duin EC, Linder D (2002) Purification and characterization of a membrane-bound enzyme complex from the sulphate-reducing archaeon Archaeglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur J Biochem 269:1895–1904

  33. Ming Y, Leyh TS (1997) Altering the reaction coordinate of the ATP Sulfurylase-GTPase reaction. Biochemistry 36(11):3270–3277

  34. Osslund T, Chandler C, Segel I (1982) ATP Sulfurylase from higher plants: purification and preliminary kinetics studies on the cabbage leaf enzyme. Plant Physiol 70(1):39–45

  35. Parey K, Demmer U, Warkentin E (2013) Structural biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS ONE. https://doi.org/10.1371/annotation/fab66ad6-bdfa-4f76-9c39-08f28a92494d

  36. Patron N, Durnford D, Kopriva S (2008) Sulfate assimilation in eukaryotes: fusions, relocations and lateral transfers. BMC Evol Biol 8:39

  37. Phartiyal P, Kim W, Cahoon R (2006) Soybean ATP sulfurylase, a homodimeric enzyme involved in sulfur assimilation, is abundantly expressed in roots and induced by cold treatment. Arch Biochem Biophys 450:20–29

  38. Pires RH, Lourenco AI, Morais F, Teixeira M, Xavier AV (2003) A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta 1605:67–82

  39. Postgate JR (1984) The sulphate-reducing bacteria, 2nd edn. Cambridge University Press, New York, 208 p

  40. Postgate JR, Campbell LL (1966) Classification of Desulfovibrio species, the non-sporulating sulfate-reducing bacteria. Bacteriol Rev 30:732–738

  41. Purish LM, Asaulenko LG, Abdulina DR, Iutinskaia GA (2014) Biodiversity of sulfate-reducing bacteria growing on objects of heating systems. Mikrobiol Zhurn 76(3):11–17

  42. Ramos AR, Keller KL, Wall JD, Pereira IA (2012) The membrane QmoABC complex interacts directly with the dissimilatory adenosine 59-phosphosulfate reductase in sulfate reducing bacteria. Front Microbiol 3:137

  43. Ravilious GE, Herrmann J, Lee SG, Westfall CS, Jez JM (2013) Kinetic mechanism of the dimeric ATP sulfurylase from plants. Biosci Rep 33(4):585–591

  44. Resonto F, Schultz T, Re E (1985) Comparative stability and catalytic and chemical properties of the sulfate-activating enzymes from Penicillium chrysogenum (mesophile) and Penicillium duponti (thermophile). J Bacteriology 164:674–683

  45. Resonto F, Patel HC, Martin RL, Thomassian C, Zimmerman G, Segel IH (1993) ATP sulfurylase from higher plants: kinetic and structural characterisation of the chloroplast and cytosol enzymes from spinach leaf. Arch Biochem Biophys 307:272–285

  46. Sakoda M, Hiromi K (1976) Determination of the best-fit values of kinetic parameters of the Michaelis-Menten equation by the method of least squares with the Taylor expansion. J Biochem 80(3):547–555

  47. Sperling D, Kappler U, Wynen A (1998) Dissimilatory ATP sulfurylase from the hyperthermopholic sulphate reducer Archaeglobus fulgidus belongs to the group of homooligomeric ATP sulfurylases. FEMS Microbiol Lett 162:257–264

  48. Widdel F (2010) Theory and Measurement of bacterial growth. Grundpraktikum Mikrobiologie, Universität Bremen 4:1–11

  49. Woordow G (1995) The Genus Desulfovibrio: the centennial. Appl Environ Microbiol 61(8):2813–2819

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This study was supported by Grant Agency of the Masaryk University (MUNI/A/0906/2017).

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Correspondence to Ivan Kushkevych.

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Abdulina, D., Kováč, J., Iutynska, G. et al. ATP sulfurylase activity of sulfate-reducing bacteria from various ecotopes. 3 Biotech 10, 55 (2020). https://doi.org/10.1007/s13205-019-2041-9

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  • Sulfate-reducing bacteria
  • ATP sulfurylase
  • Cell-free extracts
  • Ecotopes