Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress

Chi BK, Busche T, Van Laer K, Baesell K, Becher D, Clermont L, Seibold GM, Persicke M, Kalinowski J, Messens J, Antelmann H (2014)
Antioxidants & Redox Signaling 20(4): 589-605.

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Aims: Protein S-bacillithiolation was recently discovered as important thiol protection and redox-switch mechanism in response to hypochlorite stress in Firmicutes bacteria. Here we used transcriptomics to analyze the NaOCl stress response in the mycothiol (MSH)-producing Corynebacterium glutamicum. We further applied thiol-redox proteomics and mass spectrometry (MS) to identify protein S-mycothiolation. Results: Transcriptomics revealed the strong upregulation of the disulfide stress sigma(H) regulon by NaOCl stress in C. glutamicum, including genes for the anti sigma factor (rshA), the thioredoxin and MSH pathways (trxB1, trxC, cg1375, trxB, mshC, mca, mtr) that maintain the redox balance. We identified 25 S-mycothiolated proteins in NaOCl-treated cells by liquid chromatography-tandem mass spectrometry (LC-MS/MS), including 16 proteins that are reversibly oxidized by NaOCl in the thiol-redox proteome. The S-mycothiolome includes the methionine synthase (MetE), the maltodextrin phosphorylase (MalP), the myoinositol-1-phosphate synthase (Ino1), enzymes for the biosynthesis of nucleotides (GuaB1, GuaB2, PurL, NadC), and thiamine (ThiD), translation proteins (TufA, PheT, RpsF, RplM, RpsM, RpsC), and antioxidant enzymes (Tpx, Gpx, MsrA). We further show that S-mycothiolation of the thiol peroxidase (Tpx) affects its peroxiredoxin activity in vitro that can be restored by mycoredoxin1. LC-MS/MS analysis further identified 8 proteins with S-cysteinylations in the mshC mutant suggesting that cysteine can be used for S-thiolations in the absence of MSH. Innovation and Conclusion: We identified widespread protein S-mycothiolations in the MSH-producing C. glutamicum and demonstrate that S-mycothiolation reversibly affects the peroxidase activity of Tpx. Interestingly, many targets are conserved S-thiolated across bacillithiol- and MSH-producing bacteria, which could become future drug targets in related pathogenic Gram-positives.
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Chi BK, Busche T, Van Laer K, et al. Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling. 2014;20(4):589-605.
Chi, B. K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G. M., et al. (2014). Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling, 20(4), 589-605.
Chi, B. K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G. M., Persicke, M., Kalinowski, J., Messens, J., et al. (2014). Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling 20, 589-605.
Chi, B.K., et al., 2014. Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling, 20(4), p 589-605.
B.K. Chi, et al., “Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress”, Antioxidants & Redox Signaling, vol. 20, 2014, pp. 589-605.
Chi, B.K., Busche, T., Van Laer, K., Baesell, K., Becher, D., Clermont, L., Seibold, G.M., Persicke, M., Kalinowski, J., Messens, J., Antelmann, H.: Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress. Antioxidants & Redox Signaling. 20, 589-605 (2014).
Chi, Bui Khanh, Busche, Tobias, Van Laer, Koen, Baesell, Katrin, Becher, Doerte, Clermont, Lina, Seibold, Gerd M., Persicke, Marcus, Kalinowski, Jörn, Messens, Joris, and Antelmann, Haike. “Protein S-Mycothiolation Functions as Redox-Switch and Thiol Protection Mechanism in Corynebacterium glutamicum Under Hypochlorite Stress”. Antioxidants & Redox Signaling 20.4 (2014): 589-605.
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7 Citations in Europe PMC

Data provided by Europe PubMed Central.

Redox regulation by reversible protein S-thiolation in bacteria.
Loi VV, Rossius M, Antelmann H., Front Microbiol 6(), 2015
PMID: 25852656
The Corynebacterium glutamicum mycothiol peroxidase is a reactive oxygen species-scavenging enzyme that shows promiscuity in thiol redox control.
Pedre B, Van Molle I, Villadangos AF, Wahni K, Vertommen D, Turell L, Erdogan H, Mateos LM, Messens J., Mol. Microbiol. 96(6), 2015
PMID: 25766783
Corynebacterium diphtheriae methionine sulfoxide reductase a exploits a unique mycothiol redox relay mechanism.
Tossounian MA, Pedre B, Wahni K, Erdogan H, Vertommen D, Van Molle I, Messens J., J. Biol. Chem. 290(18), 2015
PMID: 25752606
Thiol-based redox switches in prokaryotes.
Hillion M, Antelmann H., Biol. Chem. 396(5), 2015
PMID: 25720121
Corynebacterium glutamicum methionine sulfoxide reductase A uses both mycoredoxin and thioredoxin for regeneration and oxidative stress resistance.
Si M, Zhang L, Chaudhry MT, Ding W, Xu Y, Chen C, Akbar A, Shen X, Liu SJ., Appl. Environ. Microbiol. 81(8), 2015
PMID: 25681179
NrdH Redoxin enhances resistance to multiple oxidative stresses by acting as a peroxidase cofactor in Corynebacterium glutamicum.
Si MR, Zhang L, Yang ZF, Xu YX, Liu YB, Jiang CY, Wang Y, Shen XH, Liu SJ., Appl. Environ. Microbiol. 80(5), 2014
PMID: 24375145

60 References

Data provided by Europe PubMed Central.

Glycogen formation in Corynebacterium glutamicum and role of ADP-glucose pyrophosphorylase.
Seibold G, Dempf S, Schreiner J, Eikmanns BJ., Microbiology (Reading, Engl.) 153(Pt 4), 2007
PMID: 17379737
Roles of maltodextrin and glycogen phosphorylases in maltose utilization and glycogen metabolism in Corynebacterium glutamicum.
Seibold GM, Wurst M, Eikmanns BJ., Microbiology (Reading, Engl.) 155(Pt 2), 2009
PMID: 19202084
Genesis: cluster analysis of microarray data.
Sturn A, Quackenbush J, Trajanoski Z., Bioinformatics 18(1), 2002
PMID: 11836235
Mycoredoxin-1 is one of the missing links in the oxidative stress defence mechanism of Mycobacteria.
Van Laer K, Buts L, Foloppe N, Vertommen D, Van Belle K, Wahni K, Roos G, Nilsson L, Mateos LM, Rawat M, van Nuland NA, Messens J., Mol. Microbiol. 86(4), 2012
PMID: 22970802
Low-molecular-weight thiols in thiol-disulfide exchange.
Van Laer K, Hamilton CJ, Messens J., Antioxid. Redox Signal. 18(13), 2013
PMID: 23075082
Redox active thiol sensors of oxidative and nitrosative stress.
Vazquez-Torres A., Antioxid. Redox Signal. 17(9), 2012
PMID: 22257022
Corynebacterium glutamicum survives arsenic stress with arsenate reductases coupled to two distinct redox mechanisms.
Villadangos AF, Van Belle K, Wahni K, Dufe VT, Freitas S, Nur H, De Galan S, Gil JA, Collet JF, Mateos LM, Messens J., Mol. Microbiol. 82(4), 2011
PMID: 22032722

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