Folia Microbiologica

, 52:120 | Cite as

Protective role of mitochondrial superoxide dismutase against high osmolarity, heat and metalloid stress inSaccharomyces cerevisiae

  • D. Dziadkowiec
  • A. Krasowska
  • A. Liebner
  • K. Sigler


Superoxide dismutases, both cytosolic Cu,Zn-SOD encoded bySOD1 and mitochondrial Mn-SOD encoded bySOD2, serveSaccharomyces cerevisiae cells for defense against the superoxide radical but the phenotypes ofsod1Δ andsod2Δ mutant strains are different. Compared with the parent strain and thesod1Δ mutant, thesod2Δ mutant shows a much more severe growth defect at elevated salt concentrations, which is partially rescued by 2 mmol/L glutathione. The growth of all three strains is reduced at 37 °C, thesod2Δ showing the highest sensitivity, especially when cultured in air. Addition of 1 mmol/L glutathione to the medium restores aerobic growth of thesod1Δ mutant but has only a minor effect on the growth of thesod2Δ strain at 37 °C. Thesod2Δ strain is also sensitive to AsIII and AsV and its sensitivity is much more pronounced under aerobic conditions. These results suggest that, unlike the Sod1p protein, whose major role is oxidative stress defense, Sod2p also plays a role in protectingS. cerevisiae cells against other stresses — high osmolarity, heat and metalloid stress.


Arsenite High Osmolarity Oxidative Stress Defense Mitochondrial Superoxide DISMUTASE Severe Growth Defect 



post-diauxic-shift (element)


reactive oxygen species


superoxide dismutase (EC


stress response (element)

Cu,Zn-SOD (SOD1)

cytosolic superoxide dismutase


mitochondrial superoxide dismutase


  1. Adamis P.D.B., Gomes D.S., Pereira M.D., Mesquita J.F., Pinto M.L.C.C., Panek A.D., Eleutherio E.C.A.: The effect of superoxide dismutase deficiency on cadmium stress.J.Biochem.Mol.Toxicol. 18, 1–6 (2004).CrossRefGoogle Scholar
  2. Avery S.V.: Metal toxicity in yeast and the role of oxidative stress.Adv.Appl.Microbiol. 49, 111–142 (2001).PubMedCrossRefGoogle Scholar
  3. Balzi E., Chen W., Ułaszewski S., Capieaux E., Goffeau A.: The multidrug resistance gene PDR1 fromSaccharomyces cerevisiae.J.Biol.Chem. 262, 16871–16879 (1987).PubMedGoogle Scholar
  4. Bobrowicz P., Wysocki R., Owsianik G., Goffeau G., Ułaszewski S.: Isolation of three contiguous genes,ACR1, ACR2 andACR3, involved in resistance to arsenic compounds in the yeastSaccharomyces cerevisiae.Yeast 13, 819–828 (1997).PubMedCrossRefGoogle Scholar
  5. Bonneaud N., Ozier-Kalogeropoulos O., Li G.Y., Labouresse M., Minvielle-Sebastia L., Lacroute F.: A family of low and high copy replicative, integrative and single-strandedS. cerevisiae/E. coli shuttle vectors.Yeast 7, 609–615 (1991).PubMedCrossRefGoogle Scholar
  6. Brennen R.J., Schiestl R.H.: Cadmium is an inducer of oxidative stress in yeast.Mutat.Res. 356, 171–178 (1996).Google Scholar
  7. Clemens S., Kim E.J., Neumann D., Schroeder J.I.: Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast.EMBO J. 18, 3325–3333 (1999).PubMedCrossRefGoogle Scholar
  8. Costa V., Amorim M.A., Reis E., Quintanilha A., Moradas-Ferreira P.: Mitochondrial superoxide dismutase is essential for ethanol tolerance of in the post-diauxic phase.Microbiology 143, 1649–1656 (1997).PubMedCrossRefGoogle Scholar
  9. Cyrne L., Martins L., Fernandes L., Marinho H.S.: Regulation of antioxidant enzymes gene expression in the yeastSaccharomyces cerevisiae during stationary phase.Free Rad.Biol.Med. 34, 385–393 (2003).PubMedCrossRefGoogle Scholar
  10. Fabrizio P., Jiou L-L., Moy V.N., Diaspro A., Valentine J.S., Gralla E.B., Longo V.D.:SOD2 functions downstream ofSch9 to extend longevity in yeast.Genetics 163, 35–46 (2003).PubMedGoogle Scholar
  11. Flattery-O’Brien J.A., Grant C.M., Dawes I.W.: Stationary-phase dependent regulation of theSaccharomyces cerevisiae SOD2 gene is dependent on additive effects of HAP2/3/4/5- and STRE-binding elements.Mol.Microbiol. 23, 303–312 (1997).PubMedCrossRefGoogle Scholar
  12. Gralla E.B., Thiele D.J., Silar P., Valentine J.S.: ACE1, a copper-dependent transcription factor, activates expression of the yeast copper, zinc superoxide dismutase gene.Proc.Nat.Acad.Sci.USA 88, 8558–8562 (1991).PubMedCrossRefGoogle Scholar
  13. Gralla E.B., Kosman D.J.: Molecular genetics of superoxide dismutases in yeast and related fungi.Adv.Genet. 30, 251–319 (1992).PubMedCrossRefGoogle Scholar
  14. Güldener U., Heck S., Fiedler T., Beinhauer J., Hegemann J.H.: A new efficient gene disruption cassette for repeated use in budding yeast.Nucl.Acids Res. 24, 2519–2524 (1996).PubMedCrossRefGoogle Scholar
  15. Hwang C.-S., Rhie G.-E., Oh J.-H.: Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection ofCandida albicans against oxidative stresses and the expression of its full virulence.Microbiology 148, 3705–3713 (2002).PubMedGoogle Scholar
  16. Hwang C.-H., Baek Y.-U., Yim H.-S., Kang S.-O.: Protective roles of mitochondrial manganese-containing superoxide dismutase against various stresses inCandida albicans.Yeast 20, 929–941 (2003).PubMedCrossRefGoogle Scholar
  17. Ito H., Fukuda Y., Murata K., Kimura A.: Transformation of intact yeast cells treated with alkali cations.J.Bacteriol. 153, 163–168 (1983).PubMedGoogle Scholar
  18. Jamieson D.J.: Oxidative stress responses of the yeastSaccharomyces cerevisiae.Yeast 14, 1511–1527 (1998).PubMedCrossRefGoogle Scholar
  19. Jeong J.-H., Kwon E.-S., Roe J.-H.: Characterization of the manganese-containing superoxide dismutase and its gene regulation in stress response ofSchizosaccharomyces pombe.Biochem.Biophys.Res.Commun. 283, 908–914 (2001).PubMedCrossRefGoogle Scholar
  20. Krasowska A., Oświęcimska M., Pasternak A., Chmielewska L., Witek S., Sigler K.: New phenolic antioxidants of PYA and PYE classes increase the resistance ofS. cerevisiae strain SP4, its SOD- and catalase-deficient mutants to lipophilic oxidants.Folia Microbiol. 44, 657–662 (1999).CrossRefGoogle Scholar
  21. Krasowska A., Łukaszewicz M., Oświęcimska M., Witek S., Sigler K.: Spontaneous and radical-induced plasma membrane lipid peroxidation in differently oxidant-sensitive yeast species and its suppression by antioxidants.Folia Microbiol. 45, 509–514 (2000).CrossRefGoogle Scholar
  22. Krasowska A., Dziadkowiec D., Łukaszewicz M., Wojtowicz K., Sigler K.: Effect of antioxidants onSaccharomyces cerevisiae mutants deficient in superoxide dismutases.Folia Microbiol. 48, 754–760 (2003).CrossRefGoogle Scholar
  23. Krasowska A., Piasecki A., Polinceusz A., Prescha A., Sigler K.: Amphiphilic amine-N-oxides with aliphatic alkyl chain act as efficient superoxide dismutase mimics, antioxidants and lipid peroxidation blockers in yeast.Folia Microbiol. 50, 99–108 (2005).CrossRefGoogle Scholar
  24. Longo V.D., Gralla E.B., Valentine J.S.: Superoxide dismutase activity is essential for stationary phase survival inSaccharomyces cerevisiae.J.Biol.Chem. 271, 12275–12280 (1996).PubMedCrossRefGoogle Scholar
  25. Pereira M.D., Herdeiro R.S., Fernandes P.N., Eleutherio E.C.A., Panek A.D.: Targets of oxidative stress in yeastsod mutants.Biochim.Biophys.Acta 1620, 245–251 (2003).PubMedGoogle Scholar
  26. Piper P.W.: The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap.FEMS Microbiol. Lett. 134, 121–127 (1995).PubMedCrossRefGoogle Scholar
  27. Rodriguez-Gabriel M.A., Russell P.: Distinct signaling pathways respond to arsenite and reactive oxygen species inSchizosaccharomyces pombe.Eukaryotic Cell 4, 1396–1402 (2005).PubMedCrossRefGoogle Scholar
  28. Saccharomyces Genome Database: Scholar
  29. Sigler K., Chaloupka J., Brozmanová J., Stadler N., Höfer M.: Oxidative stress in microorganisms. I. Microbialversus higher cells — damage and defenses in relation to cell aging and death.Folia Microbiol. 44, 587–624 (1999).CrossRefGoogle Scholar
  30. Sturtz L.A., Diekert K., Jensen L.T., Lill R., Culotta V.C.: A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localized to the intermembrane space of mitochondria.J.Biol.Chem. 276, 38084–38089 (2001).PubMedGoogle Scholar
  31. Sturtz L.A., Culotta V.C.: Superoxide dismutase null mutants of baker’s yeast,Saccharomyces cerevisiae.Meth.Enzymol. 349, 167–172 (2002).PubMedCrossRefGoogle Scholar
  32. Sugiyama K., Izawa S., Inoue Y.: The Yaplp-dependent induction of glutathione synthesis in heat shock response ofSaccharomyces cerevisiae.J.Biol.Chem. 275, 15535–15540 (2000).PubMedCrossRefGoogle Scholar
  33. Wallace M.A., Jiou L.-L., Martins J., Clement M.H.S., Bailey S., Longo V.D., Valentine J.S., Gralla E.B.: Superoxide inhibits 4Fe-4S cluster enzymes involved in amino acid biosynthesis.J.Biol.Chem. 279, 32055–32062 (2004).PubMedCrossRefGoogle Scholar
  34. Wysocki R., Clemens S., Augustyniak D., Golik P., Maciaszczyk E., Tamas M.J., Dziadkowiec D.: Metalloid tolerance based on phytochelatins is not functionally equivalent to the arsenite transporter Acr3p.Biochem.Biophys.Res.Commun. 304, 293–300 (2003).PubMedCrossRefGoogle Scholar
  35. Wysocki R., Fortier P.-K., Maciaszczyk E., Thorsen M., Leduc A., Odhagen A., Owsianik G., Ułaszewski S., Ramotar D., Tamas M.J.: Transcriptional activation of metalloid tolerance genes inSaccharomyces cerevisiae requires the AP-1-like proteins Yap1p and Yap8p.Mol.Biol.Cell 15, 2049–2060 (2004).PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic 2007

Authors and Affiliations

  • D. Dziadkowiec
    • 1
  • A. Krasowska
    • 1
  • A. Liebner
    • 1
  • K. Sigler
    • 2
  1. 1.Faculty of BiotechnologyWrocław UniversityWrocławPoland
  2. 2.Institute of MicrobiologyAcademy of Sciences of the Czech RepublicPragueCzechia

Personalised recommendations