Changes in Activity of Antioxidant Systems of Escherichia coli under Phosphate Starvation

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Дәйексөз келтіру

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Аннотация

Changes in the activity of antioxidant systems in Escherichia coli during phosphate starvation were studied. It was shown that starvation was accompanied by a decrease in the intensity of respiration, an increase in the rate of superoxide production, and a decrease in the level of ATP. Simultaneously, there was a decrease in H2O2 in the medium and a significant increase in the expression of the katG and katE genes encoding the HPI and HPII catalases, respectively. At the same time, there was no drop in the membrane potential, which may indicate the retention of normal membrane activity in starving cells. It has been shown for the first time that the transition of E. coli to phosphate starvation is accompanied by significant changes in the status of glutathione. The most important of them are associated with a decrease in the level of glutathione reductive form (GSH) in the medium (GSHout) and with a simultaneous increase in its content in the cytoplasm (GSHin), as well as a shift in the GSHin to oxidized glutathione form (GSSGin) ratio towards reductive values, and GSHout/GSSGout towards oxidative values. Among the mutants used in the work, the double mutant gor trxB, deficient in the synthesis of glutathione reductase and thioredoxin reductase, showed the most pronounced distinctive features. Compared to the parental strain, this mutant showed a multiple higher expression of katG::lacZ, the highest level of oxidized intra- and extracellular glutathione, and, accordingly, the lowest GSH/GSSG ratio in both compartments. In general, the data obtained indicate that during phosphate starvation the interaction of the glutathione redox-system and regulons that control protection against reactive oxygen species creates conditions that allow maintaining the concentration of ROS below the toxic level. As a result, phosphate-starved E. coli cells can maintain a high viability for a long time that allows them quickly to resume growth after the addition of phosphate.

Авторлар туралы

G. Smirnova

Institute of Ecology and Genetics of Microorganisms, “Perm Federal Research Center”,
Ural Branch, Russian Academy of Sciences

Email: oktyabr@iegm.ru
Russia, 614081, Perm

A. Tyulenev

Institute of Ecology and Genetics of Microorganisms, “Perm Federal Research Center”,
Ural Branch, Russian Academy of Sciences

Email: oktyabr@iegm.ru
Russia, 614081, Perm

N. Muzyka

Institute of Ecology and Genetics of Microorganisms, “Perm Federal Research Center”,
Ural Branch, Russian Academy of Sciences

Email: oktyabr@iegm.ru
Russia, 614081, Perm

L. Sutormina

Institute of Ecology and Genetics of Microorganisms, “Perm Federal Research Center”,
Ural Branch, Russian Academy of Sciences

Email: oktyabr@iegm.ru
Russia, 614081, Perm

O. Oktyabrsky

Institute of Ecology and Genetics of Microorganisms, “Perm Federal Research Center”,
Ural Branch, Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: oktyabr@iegm.ru
Russia, 614081, Perm

Әдебиет тізімі

  1. Sevilla E., Bes M.T., Gonzalez A., Peleato M.L., Fillat M.F. (2019) Redox-based transcriptional regulation in prokaryotes: revisiting model mechanisms. Antioxid. Redox Signal. 30, 1651–1696. https://doi.org/10.1089/ars.2017.7442
  2. Imlay J.A. (2008) Cellular defenses against superoxide and hydrogen peroxide. Ann. Rev. Biochem. 77, 755–776. https://doi.org/10.1146/annurev.biochem.77.061606.161055
  3. Смирнова Г.В., Октябрьский О.Н. (2005) Глутатион у бактерий. Биохимия. 70, 1459– 1473.
  4. Vlamis-Gardikas A. (2008) The multiple functions of the thiol-based electron flow pathways of Escherichia coli: eternal concepts revised. Biochim. Biophys. Acta. 1780, 1170–1200. https://doi.org/10.1016/j.bbagen.2008.03.013
  5. Smirnova G., Muzyka N., Oktyabrsky O. (2012) Transmembrane glutathione cycling in growing Escherichia coli cells. Microbiol. Res. 167, 166–172. https://doi.org/10.1016/j.micres.2011.05.005
  6. Carmel-Harel O., Storz G. (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu. Rev. Microbiol. 54, 439–461. https://doi.org/10.1146/annurev.micro.54.1.439
  7. Wanner B.L. (1996) Phosphorus assimilation and control of the phosphate regulon. In: Escherichia coli and Salmonella: Cellular and Molecular Biology. Eds Neidhardt F.C., Curtiss III R., Ingraham J.L., Lin E.C.C., Low K.B., Magasanik B., Reznikoff W.S., Riley M., Schaechter M., Umbrager H.E. Washington DC: Am. Soc. Microbiol., pp. 1357–1381.
  8. Lamarche M.G., Wanner B.L., Crepin S., Harel J. (2008) The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 32(3), 461–473. https://doi.org/10.1111/j.1574-6976.2008.00101.x
  9. VanBogelen R.A., Olson E.R., Wanner B.L., Neidhardt F.C. (1996) Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J. Bacteriol. 178(15), 4344–4366. https://doi.org/10.1128/jb.178.15.4344-4366.1996
  10. Gerard F., Dri A.M., Moreau P.L. (1999) Role of Escherichia coli RpoS, LexA and H-NS global regulators in metabolism and survival under aerobic, phosphate-starvation conditions. Microbiology. 145, 1547–1562. https://doi.org/10.1099/13500872-145-7-1547
  11. Moreau P.L., Gerard F., Lutz N.W., Cozzone P. (2001) Non-growing Escherichia coli cells starved for glucose or phosphate use different mechanisms to survive oxidative stress. Mol. Microbiol. 39, 1048–1060. https://doi.org/10.1046/j.1365-2958.2001.02303.x
  12. Moreau P.L. (2004) Diversion of the metabolic flux from pyruvate dehydrogenase to pyruvate oxidase decreases oxidative stress during glucose metabolism in nongrowing Escherichia coli cells incubated under aerobic, phosphate starvation conditions. J. Bacteriol. 186, 7364–7368. https://doi.org/10.1128/JB.186.21.7364-7368.2004
  13. Yuan Z.C., Zaheer R., Finan T.M. (2005) Phosphate limitation induces catalase expression in Sinorhizobium meliloti, Pseudomonas aeruginosa and Agrobacterium tumefaciens. Mol. Microbiol. 58(3), 877–894. https://doi.org/10.1111/j.1365-2958.2005.04874.x
  14. Smirnova G.V., Tyulenev A.V., Bezmaternykh K.V., Muzyka N.G., Ushakov V.Y., Oktyabrsky O.N. (2019) Cysteine homeostasis under inhibition of protein synthesis in Escherichia coli cells. Amino Acids. 51, 1577–1592. https://doi.org/10.1007/s00726-019-02795-2
  15. Park S., Imlay, J.A. (2003) High levels of intracellular cysteine promote oxidative DNA damage by driving the Fenton reaction. J. Bacteriol. 185, 1942–1950. https://doi.org/10.1128/JB.185.6.1942-1950.2003
  16. Imlay K.R.C., Korshunov S., Imlay J.A. (2015) The physiological roles and adverse effects of the two cystine importers of Escherichia coli. J. Bacteriol. 197, 3629–3644. https://doi.org/10.1128/JB.00277-15
  17. Korshunov S., Imlay K.R.C., Imlay J.A. (2020) Cystine import is a valuable but risky process whose hazards Escherichia coli minimizes by inducing a cysteine exporter. Mol. Microbiol. 113, 22–39. https://doi.org/10.1111/mmi.14403
  18. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008. https://doi.org/10.1038/msb4100050
  19. Tao K., Makino K., Yonei S., Nacata A., Shinagawa H. (1989) Molecular cloning and nucleotide sequencing of oxyR, the positive regulatory gene of a regulon for an adaptive response to oxidative stress in Escherichia coli: homologies between OxyR protein and a family of bacterial activator proteins. Mol. Gen. Genet. 218, 371–376. https://doi.org/10.1007/bf00332397
  20. Mulvey M.R., Switala J., Borys A., Loewen P.C. (1990) Regulation of transcription of katE and katF in Escherichia coli. J. Bacteriol. 172, 6713–6720. https://doi.org/10.1128/jb.172.12.6713-6720.1990
  21. Volkert M.R., Gately F.H., Hajec L.I. (1989) Expression of DNA damage-inducible genes of Escherichia coli upon treatment with methylating, ethylating and propylating agents. Mutation. Res. 217, 109–115. https://doi.org/10.1016/0921-8777(89)90062-1
  22. Maringanti S., Imlay J.A. (1999) An intracellular iron chelator pleiotropically suppresses enzymatic and growth defects of superoxide dismutase-deficient Escherichia coli. J. Bacteriol. 181, 3792–3802. https://doi.org/10.1128/JB.181.12.3792-3802.1999
  23. Neidhardt F.C., Bloch P.L., Smith D.F. (1974) Culture medium for enterobacteria. J. Bacteriol. 119, 736–747. https://doi.org/10.1128/jb.119.3.736-747.1974
  24. Wickens H.J., Pinney R.J., Mason D.J., Gant V.A. (2000) Flow cytometric investigation of filamentation, membrane patency and membrane potential in Escherichia coli following ciprofloxacin exposure. Antimicrob. Agents Chemother. 44, 682–687. https://doi.org/10.1128/AAC.44.3.676-681.2000
  25. Smirnova G.V., Muzyka N.G., Ushakov V.Y., Tyulenev A.V., Oktyabrsky O.N. (2015) Extracellular superoxide provokes glutathione efflux from Escherichia coli cells. Res. Microbiol. 166, 609–617. https://doi.org/10.1016/j.resmic.2015.07.007
  26. Korshunov S., Imlay J.A. (2006) Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J. Bacteriol. 188, 6326–6334. https://doi.org/10.1128/JB.00554-06
  27. Seaver L.C., Imlay J.A. (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183, 7173–7181. https://doi.org/10.1128/JB.183.24.7173-7181.2001
  28. Tietze F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and ot-her tissues. Anal. Biochem. 27, 502–522. https://doi.org/10.1016/0003-2697(69)90064-5
  29. Miller J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Lab. Press.
  30. Ivanova A., Miller C., Glinsky G., Eisenstark A. (1994) Role of the rpoS(katF) in oxyR independent regulation of hydroperoxidase I in Escherichia coli. Mol. Microbiol. 12, 571–578. https://doi.org/10.1111/j.1365-2958.1994.tb01043.x
  31. Ihssen J., Egli T. (2004) Specific growth rate and not cell density controls the general stress response in Escherichia coli. Microbiology. 150, 1637–1648. https://doi.org/10.1099/mic.0.26849-0
  32. Imlay J.A., Linn S. (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science. 240, 640–642. https://doi.org/10.1126/science.2834821
  33. Hantke K. (2001) Iron and metal regulation in bacteria. Curr. Opin. Microbiol. 4, 172–177. https://doi.org/10.1016/s1369-5274(00)00184-3
  34. Maslowska K.H., Makiela-Dzbenska K., Fijalkowska I.J. (2019) The SOS system: a complex and tightly regulated response to DNA damage. Environ. Mol. Mutagen. 60, 368–384. https://doi.org/10.1002/em.22267
  35. Tyulenev A.V., Smirnova G.V., Muzyka N.G., Ushakov V.Y., Oktyabrsky O.N. (2018) The role of sulfides in stress-induced changes of Eh in Escherichia coli cultures. Bioelectrochemistry. 121, 11–17. https://doi.org/10.1016/j.bioelechem.2017.12.012
  36. Smirnova G.V., Tyulenev A.V., Muzyka N.G., Oktyabrsky O.N. (2018) The sharp phase of respiratory inhibition during amino acid starvation in Escherichia coli is RelA-dependent and associated with regulation of ATP synthase activity. Res. Microbiol. 169, 157–165. https://doi.org/10.1016/j.resmic.2018.02.003
  37. Owens R.A., Hartman P.E. (1986) Export of glutathione by some widely used Salmonella typhimurium and Escherichia coli strains. J. Bacteriol. 168, 109–114. https://doi.org/10.1128/jb.168.1.109-114.1986
  38. Imlay J.A. (2013) The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat. Rev. Microbiol. 11, 443–454. https://doi.org/10.1038/nrmicro3032
  39. Aslund F., Zheng M., Beckwith J., Storz G. (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl. Acad. Sci. USA. 96, 6161–6165. https://doi.org/10.1073/pnas.96.11.6161
  40. Smirnova G.V., Tyulenev A.V., Muzyka N.G., Peters M.A., Oktyabrsky O.N. (2017) Ciprofloxacin provokes SOS-dependent changes in respiration and membrane potential and causes alterations in the redox status of Escherichia coli. Res. Microbiol. 168, 64–73. https://doi.org/10.1016/j.resmic.2016.07.008
  41. Smirnova G.V., Tyulenev A.V., Muzyka N.G., Oktyabrsky O.N. (2022) Study of the contribution of active defense mechanisms to ciprofloxacin tolerance in Escherichia coli growing at different rates. Antonie Van Leeuwenhoek. 115, 233–251. https://doi.org/10.1007/s10482-021-01693-6
  42. Smirnova G., Tyulenev A., Muzyka N., Ushakov V., Samoilova Z., Oktyabrsky O. (2023) Influence of growth medium composition on physiological responses of Escherichia coli to the action of chloramphenicol and ciprofloxacin. BioTech. 12, 43. https://doi.org/10.3390/biotech12020043

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