Stress-Induced Sulfide Production by Bacillus subtilis and Bacillus megaterium
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strains and Growth Conditions
2.2. Real-Time Monitoring of Eh, Dissolved Oxygen (dO2), pH, and Ions of Extracellular Sulfide (S2−) and Potassium (K+)
2.3. Determination of Intracellular and Extracellular Cysteine
2.4. Determination of Total Catalase Activity
2.5. Statistical Analysis of the Data
3. Results
3.1. Glucose and Ammonium Depletion in B. subtilis and E. coli
3.2. Exposure of B. subtilis to Antibiotics
3.3. Response of B. subtilis to the Addition of Cystine
3.4. Catalase Activity in B. subtilis and E. coli
3.5. H2S Excretion in B. megaterium
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Oktyabrskii, O.N.; Smirnova, G.V. Redox potential changes in bacterial cultures under stress conditions. Microbiology 2012, 81, 131–142. [Google Scholar] [CrossRef]
- Tyulenev, A.; Smirnova, G.; Muzyka, N.; Ushakov, V.; Oktyabrsky, O. The role of sulfides in stress-induced changes of Eh in Escherichia coli cultures. Bioelectrochemistry 2018, 121, 11–17. [Google Scholar] [CrossRef]
- Smirnova, G.V.; Tyulenev, A.V.; Bezmaternykh, K.V.; Muzyka, N.G.; Ushakov, V.Y.; Oktyabrsky, O.N. Cysteine homeostasis under inhibition of protein synthesis in Escherichia coli cells. Amino Acids 2019, 51, 1577–1592. [Google Scholar] [CrossRef] [PubMed]
- Tanaka, N.; Hatanom, T.; Saito, S.Y.W.; Abe, T.; Kawano, Y.; Ohtsu, I. Generation of hydrogen sulfide from sulfur assimilation in Escherichia coli. J. Gen. Appl. Microbiol. 2019, 65, 234–239. [Google Scholar] [CrossRef]
- Sorensen, M.A.; Pedersen, S. Cysteine, even in low concentrations, induces transient amino acid starvation in Escherichia coli. J. Bacteriol. 1991, 173, 5244–5246. [Google Scholar] [CrossRef] [PubMed]
- Park, S.; Imlay, J.A. High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 2003, 185, 1942–1950. [Google Scholar] [CrossRef]
- Kredich, N.M. Biosynthesis of cysteine. EcoSal Plus 2008, 3. [Google Scholar] [CrossRef]
- Kimura, H. Production and physiological effects of hydrogen sulfide. Antioxid. Redox. Signal. 2014, 20, 783–793. [Google Scholar] [CrossRef]
- Shatalin, K.; Shatalina, E.; Mironov, A.; Nudler, E. A universal defense against antibiotics in bacteria. Science 2011, 334, 986–990. [Google Scholar] [CrossRef]
- Mironov, E.; Seregina, T.; Nagornykh, M.; Luhachack, L.G.; Korolkova, N.; Lopes, L.E.; Kotova, V.; Zavilgelsky, G.; Shakulov, R.; Shatalin, K.; et al. Mechanism of H2S-mediated protection against oxidative stress in Escherichia coli. Proc. Natl. Acad. Sci. USA 2017, 114, 6022–6027. [Google Scholar] [CrossRef]
- Toliver-Kinsky, T.; Cui, W.; Törö, G.; Lee, S.-J.; Shatalin, K.; Nudler, E.; Szabo, C. H2S, a bacterial defense mechanism against the host immune response. Infect. Immun. 2018, 87, e00272-18. [Google Scholar] [CrossRef]
- Shatalin, K.; Nuthanakanti, A.; Kaushik, A.; Shishov, D.; Peselis, A.; Shamovsky, I.; Pani, B.; Lechpammer, M.; Vasilyev, N.; Shatalina, E.; et al. Inhibitors of bacterial H2S biogenesis targeting antibiotic resistance and tolerance. Science 2021, 372, 1169–1175. [Google Scholar] [CrossRef]
- Miller, J.H. Experiments in Molecular Genetics; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, USA, 1972. [Google Scholar]
- Smirnova, G.V.; Tyulenev, A.; Sutormina, L.; Kalashnikova, T.; Muzyka, N.; Ushakov, V.; Samoilova, Z.; Oktyabrsky, O. Regulation of cysteine homeostasis and its effect on Escherichia coli sensitivity to ciprofloxacin in LB medium. Int. J. Mol. Sci. 2024, 25, 4424. [Google Scholar] [CrossRef] [PubMed]
- Visick, J.E.; Clarke, S. RpoS- and OxyR-independent induction of HPI catalase of stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J. Bacteriol. 1997, 179, 4158–4163. [Google Scholar] [CrossRef]
- Ransmeier, J.C.; Stekol, J.A. Production of hydrogen sulfide from sulfur-containing compounds by various bacteria. II. Experiments with synthetic medium. Proc. Soc. Exp. Biol. Med. 1942, 51, 92–94. [Google Scholar] [CrossRef]
- Korshunov, S.; Imlay, K.R.C.; Imlay, J.A. The cytochrome bd oxidase of Escherichia coli prevents respiratory inhibition by endogenous and exogenous hydrogen sulfide. Mol. Microbiol. 2016, 101, 62–77. [Google Scholar] [CrossRef] [PubMed]
- Ohtsu, I.; Wiriyathanawudhiwong, N.; Morigasaki, S.; Nakatani, T.; Kadokura, H.; Takagi, H. The L-cysteine/L-cystine shuttle system provides reducing equivalents to the periplasm in Escherichia coli. J. Biol. Chem. 2010, 285, 17479–17487. [Google Scholar] [CrossRef]
- Imlay, K.R.C.; Korshunov, S.; Imlay, J.A. Physiological roles and adverse effects of the two cystine importers of Escherichia coli. J. Bacteriol. 2015, 19, 3629–3644. [Google Scholar] [CrossRef] [PubMed]
- Auger, S.; Danchin, A.; Martin-Verstraete, I. Global expression profile of Bacillus subtilis grown in the presence of sulfate or methionine. J. Bacteriol. 2000, 184, 5179–5186. [Google Scholar] [CrossRef]
- Burguière, P.; Auger, S.; Hullo, M.F.; Danchin, A.; Martin-Verstraete, I. Three different systems participate in L-cystine uptake in Bacillus subtilis. J. Bacteriol. 2004, 186, 4875–4884. [Google Scholar] [CrossRef]
- Even, S.; Burguière, P.; Auger, S.; Soutourina, O.; Danchin, A.; Martin-Verstraete, I. Global control of cysteine metabolism by CymR in Bacillus subtilis. J. Bacteriol. 2006, 188, 2184–2197. [Google Scholar] [CrossRef] [PubMed]
- Tanous, C.; Soutourina, O.; Raynal, B.; Hullo, M.-F.; Mervelet, P.; Gilles, A.M.; Noirot, P.; Danchin, A.; England, P.; Martin-Verstraete, I. The CymR regulator in complex with the enzyme CysK controls cysteine metabolism in Bacillus subtilis. J. Biol. Chem. 2008, 283, 35551–35560. [Google Scholar] [CrossRef] [PubMed]
- Fahey, R.C.; Brown, W.C.; Adams, W.B.; Worsham, M.B. Occurrence of glutathione in bacteria. J. Bacteriol. 1978, 133, 1126–1129. [Google Scholar] [CrossRef]
- Loewen, P.C. Levels of glutathione in Escherichia coli. Can. J. Biochem. 1979, 57, 107–111. [Google Scholar] [CrossRef]
- Smirnova, G.V.; Oktyabrsky, O.N. Glutathione in bacteria. Biochemistry 2005, 70, 1199–1211. [Google Scholar] [CrossRef] [PubMed]
- Newton, G.L.; Rawat, M.; La Clair, J.J.; Jothivasan, V.K.; Budiarto, T.; Hamilton, C.J.; Claiborne, A.; Helmann, J.D.; Fahey, R.C. Bacillithiol is an antioxidant thiol produced in Bacilli. Nat. Chem. Biol. 2009, 5, 625–627. [Google Scholar] [CrossRef]
- Chandrangsu, P.; Antelmann, H.; Loi, V.V.; Helmann, J.D. The role of bacillithiol in gram-positive firmicute. Antioxid. Redox Signal. 2018, 28, 445–462. [Google Scholar] [CrossRef]
- Newton, L.; Arnold, K.; Price, M.S.; Sherrill, C.; Delcardayre, S.B.; Aharonovitz, Y.; Cohen, G.; Davies, J.; Fahey, R.C.; Davis, C. Distribution of thiols in microorganisms: Mycothiol is a major thiol in most actinomycetes. J. Bacteriol. 1996, 178, 1990–1995. [Google Scholar] [CrossRef]
- Fahey, R.C. Glutathione analogs in prokaryotes. Biochim. Biophys. Acta 2013, 1830, 3182–3198. [Google Scholar] [CrossRef]
- Schaeffer, P.; Millet, J.; Aubert, J.P. Catabolic repression of bacterial sporulation. Proc. Nat. Acad. Sci. USA 1965, 54, 704–711. [Google Scholar] [CrossRef]
- Muyzer, G.; Stams, A.J.M. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 2008, 6, 441–454. [Google Scholar] [CrossRef] [PubMed]
- Barton, L.L.; Fauque, G.D. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv. Appl. Microbiol. 2009, 68, 41–98. [Google Scholar] [CrossRef] [PubMed]
- López-Bucio, J.; Campos-Cuevas, J.C.; Hernández-Calderón, E.; Velásquez-Becerra, C.; Farías-Rodríguez, R.; Macías-Rodríguez, L.I.; Valencia-Cantero, E. Bacillus megaterium Rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 2007, 20, 207–217. [Google Scholar] [CrossRef] [PubMed]
- Hashem, A.; Tabassum, B.; Allah, E.F.A. Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi J. Biol. Sci. 2019, 26, 1291–1297. [Google Scholar] [CrossRef]
- Hyder, S.; Rizvi, Z.F.; Santos-Villalobos, S.; Santoyo, G.; Gondal, A.S.; Khalid, N.; Fatima, S.N.; Nadeem, M.; Rafique, K.; Rani, A. Applications of plant growth-promoting rhizobacteria for increasing crop production and resilience. J. Plant Nutr. 2023, 46, 2551–2580. [Google Scholar] [CrossRef]
- Calderwood, A.; Kopriva, S. Hydrogen sulfide in plants: From dissipation of excess sulfur to signaling molecule. Nitric Oxide 2014, 41, 72–78. [Google Scholar] [CrossRef]
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Tyulenev, A.; Smirnova, G.; Ushakov, V.; Kalashnikova, T.; Sutormina, L.; Oktyabrsky, O. Stress-Induced Sulfide Production by Bacillus subtilis and Bacillus megaterium. Microorganisms 2024, 12, 1856. https://doi.org/10.3390/microorganisms12091856
Tyulenev A, Smirnova G, Ushakov V, Kalashnikova T, Sutormina L, Oktyabrsky O. Stress-Induced Sulfide Production by Bacillus subtilis and Bacillus megaterium. Microorganisms. 2024; 12(9):1856. https://doi.org/10.3390/microorganisms12091856
Chicago/Turabian StyleTyulenev, Alexey, Galina Smirnova, Vadim Ushakov, Tatyana Kalashnikova, Lyubov Sutormina, and Oleg Oktyabrsky. 2024. "Stress-Induced Sulfide Production by Bacillus subtilis and Bacillus megaterium" Microorganisms 12, no. 9: 1856. https://doi.org/10.3390/microorganisms12091856