Abstract
Sulfate-reducing bacteria (SRB) belonging to the intestinal microbiota are the main producers of hydrogen sulfide and their increasing amount due to the accumulation of this compound in the bowel are involved in the initiation and maintenance of inflammatory bowel disease. The purpose of this experiment is to study the relative toxicity of hydrogen sulfide and survival of Desulfovibrio piger Vib-7 through monitoring: sulfate reduction parameters (sulfate consumption, hydrogen sulfide production, lactate consumption and acetate production) and kinetic parameters of these processes. The research is highlighting the survival of intestinal SRB, D. piger Vib-7 under the influence of different hydrogen sulfide concentrations (1–7 mM). The highest toxicity of H2S was measured in the presence of concentrations higher than 6 mM, where growing was stopped, though metabolic activities were not 100% inhibited. These findings are confirmed by cross correlation and principal component analysis that clearly supported the above mentioned results. The kinetic parameters of bacterial growth and sulfate reduction were inhibited proportionally with increasing H2S concentration. The presence of 5 mM H2S resulted in two times longer lag phase and generation time was eight times longer. Maximum rate of growth and hydrogen production was stopped under 4 mM, emphasizing the H2S toxicity concentrations to be < 4 mM, even for sulfide producing bacteria such as Desulfovibrio. The results are confirming H2S concentrations toxicity toward Desulfovibrio, especially the study novelty should be emphasized where it was found that the exact H2S limits (> 4 mM) toward this bacterial strain inhabiting humans and animals intestine.
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Abbreviations
- SRB:
-
Sulfate-reducing bacteria
- UC:
-
Ulcerative colitis
- IBD:
-
Inflammatory bowel disease
- DSR:
-
Dissimilatory sulfate reduction
- OD:
-
Optical density
- PCA:
-
Principal component analysis
References
Attene-Ramos MS, Wagner ED, Plewa MJ, Gaskins HR (2006) Evidence that hydrogen sulfide is a genotoxic agent. Mol Cancer Res 4:9–14
Bailey NTJ (1995) Statistical methods in biology. Cambridge University Press, Cambridge
Bailey TS, Pluth MD (2013) Chemiluminescent detection of enzymatically produced hydrogen sulfide: substrate hydrogen bonding influences selectivity for H S over biological thiols. J Am Chem Soc 135(44):16697–16704
Barton LL, Hamilton WA (2010) Sulphate-reducing bacteria. Environmental and engineered systems. Cambridge University Press, Cambridge
Beauchamp RO, Bus JS, Popp JA, Boreiko CJ, Andjelkovich DA, Leber P (1984) A critical review of the literature on hydrogen sulfide toxicity. CRC Crit Rev Toxicol 13:25–97
Blachier F, Davila AM, Mimoun S (2010) Luminal sulfide and large intestine mucosa: friend or foe? Amino Acids 39:335–347
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
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural water. Limnol Ocean 14:454–458
Cummings JH, Macfarlane GT, Macfarlane S (2003) Intestinal bacteria and ulcerative colitis. Curr Issues Intest Microbiol 4:9–20
Florin TH, Neale G, Goretski S, Cummings JH (1993) Sulfate in food and beverages. J Food Compos Anal 6:140–151
Gibson GR, Cummings JH, Macfarlane GT (1991) Growth and activities of sulphate-reducing bacteria in gut contents of health subjects and patients with ulcerative colitis. FEMS Microbiol Ecol 86:103–112
Gibson GR, Macfarlane S, Macfarlane GT (1993) Metabolic interactions involving sulphate-reducing and methanogenic bacteria in the human large intestine. FEMS Microbiol Ecol 12:117–125
Griesbeck C, Schutz M, Schodl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002a) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565
Griesbeck C, Schütz M, Schödl T, Bathe S, Nausch L, Mederer N, Vielreicher M, Hauska G (2002b) Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565
Grieshaber MK, Völkel S (1998) Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu Rev Physiol 60:33–53
Kolmert A, Wikstrom P, Hallberg KB (2000) A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J Microbiol Methods 41:179–184
Kováč J, Kushkevych I (2017) New modification of cultivation medium for isolation and growth of intestinal sulfate-reducing bacteria. In: Proceeding of international Ph.D. students conference MendelNet, pp 702–707
Kováč J, Vítězová M, Kushkevych I (2018) Metabolic activity of sulfate-reducing bacteria from rodents with colitis. Open Med 13:344–349
Kushkevych IV (2013) Identification of sulfate-reducing bacteria strains of human large intestine. Studia Biologia 7:115–124
Kushkevych IV (2015a) Activity and kinetic properties of phosphotransacetylase from intestinal sulfate-reducing bacteria. Acta Biochemica Polonica 62:1037–1108
Kushkevych IV (2015b) Kinetic properties of pyruvate ferredoxin oxidoreductase of intestinal sulfate-reducing bacteria Desulfovibrio piger Vib-7 and Desulfomicrobium sp. Rod-9. Pol J Microbiol 64:107–114
Kushkevych I, Bartos M, Bartosova L (2014) Sequence analysis of the 16S rRNA gene of sulfate-reducing bacteria isolated from human intestine. Int J Curr Microbiol Appl Sci 3:239–248
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
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
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
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
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
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
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
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
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
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
Loubinoux J, Mory F, Pereira IA, Le Faou AE (2000) Bacteremia caused by a strain of Desulfovibrio related to the provisionally named Desulfovibrio fairfieldensis. J Clin Microbiol 38:931–934
Loubinoux J, Bronowicji JP, Pereira IA (2002a) Sulphate-reducing bacteria in human feces and their association with inflammatory diseases. FEMS Microbiol Ecol 40:107–112
Loubinoux J, Valente FMA, Pereira IAC (2002b) Reclassification of the only species of the genus Desulfomonas, Desulfomonas pigra, as Desulfovibrio piger comb. nov. Int J of Syst Evol Microbiol 52:1305–1308
Pitcher MC, Cummings JH (1996) Hydrogen sulphide: a bacterial toxin in ulcerative colitis? Gut 39, 1–4
Postgate JR (1984) The sulfate-reducing bacteria. Cambridge University Press, Cambridge
Rowan FE, Docherty NG, Coffey JC, O’Connell PR (2009) Sulphate-reducing bacteria and hydrogen sulphide in the aetiology of ulcerative colitis. Br J Surg 96:151–158
Acknowledgements
This study was supported by Grant Agency of the Masaryk University (MUNI/A/0902/2018).
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IK, DD, MV wrote the article. All authors contributed to the conception, design and critically revised the manuscript.
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Communicated by Erko Stackebrandt.
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Kushkevych, I., Dordević, D. & Vítězová, M. Toxicity of hydrogen sulfide toward sulfate-reducing bacteria Desulfovibrio piger Vib-7. Arch Microbiol 201, 389–397 (2019). https://doi.org/10.1007/s00203-019-01625-z
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DOI: https://doi.org/10.1007/s00203-019-01625-z