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Oversynthesis of Riboflavin in the Yeast Pichia guilliermondii is Accompanied by Reduced Catalase and Superoxide Dismutases Activities

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Abstract

Iron deficiency causes oversynthesis of riboflavin in several yeast species, known as flavinogenic yeasts. Under iron deprivation conditions, Pichia guilliermondii cells increase production of riboflavin and malondialdehyde and the formation of protein carbonyl groups, which reflect increased intracellular content of reactive oxygen species. In this study, we found that P. guilliermondii iron deprived cells showed dramatically decreased catalase and superoxide dismutase activities. Previously reported mutations rib80, rib81, and hit1, which affect repression of riboflavin synthesis and iron accumulation by iron ions, caused similar drops in activities of the mentioned enzymes. These findings could explain the previously described development of oxidative stress in iron deprived or mutated P. guilliermondii cells that overproduce riboflavin. Similar decrease in superoxide dismutase activities was observed in iron deprived cells in the non-flavinogenic yeast Saccharomyces cerevisiae.

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References

  1. Abbas CA, Sibirny AA (2011) Genetic control of biosynthesis and transport of riboflavin and flavin nucleotides and construction of robust biotechnological producers. Microbiol Mol Biol Rev 75:321–360

    Article  PubMed  CAS  Google Scholar 

  2. Boretsky Y, Protchenko O, Prokopiv T, Mukalov I, Fedorovych D, Sibirny A (2007) Mutations and environmental factors affecting regulation of riboflavin synthesis and iron assimilation also cause oxidative stress in the yeast Pichia guilliermondii. J Basic Microbiol 47:371–377

    Article  PubMed  CAS  Google Scholar 

  3. Bridges SM, Salin ML (1981) Distribution of iron-containing superoxide dismutase in vascular plants. Plant Physiol 68:275–278

    Article  PubMed  CAS  Google Scholar 

  4. Chauhan N, Latge JP, Calderone R (2006) Signalling and oxidant adaptation in Candida albicans and Aspergillus fumigatus. Nat Rev Microbiol 4:435–444

    Article  PubMed  CAS  Google Scholar 

  5. Cizewski-Culotta V, Klomp LWJ, Strain J et al (1997) The copper chaperone for superoxide dismutase. J Biol Chem 272:23469–23472

    Article  Google Scholar 

  6. Cohen G, Fessl F, Traczyk A, Rytka J, Ruis H (1985) Isolation of the catalase A gene of Saccharomyces cerevisiae by complementation of the ctal mutation. Mol Gen Genet 200:74–79

    Article  PubMed  CAS  Google Scholar 

  7. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329:23–38

    Article  PubMed  CAS  Google Scholar 

  8. Davidson JF, Whyte B, Bissinger PH, Schiestl RH (1996) Oxidative stress is involved in heat-induced cell death in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 93:5116–5121

    Article  PubMed  CAS  Google Scholar 

  9. Enary TM (1955) Effect of cobalt and iron on riboflavin by Candida guilliermondii. Acta Chem Scand 9:19–23

    Google Scholar 

  10. Fedorovich DV, Kityk IV, Dzhala VI, Protchenko OV, Shavlovskii GM (1997) Accumulation and redox transformations of iron in the yeast Pichia guilliermondii and its flavinogenic mutants. Mikrobiologiya 66:48–51 (in Russian)

    CAS  Google Scholar 

  11. Fedorovich D, Protchenko O, Lesuisse E (1999) Iron uptake by the yeast Pichia guilliermondii. Flavinogenesis and reductive iron assimilation are co-regulated processes. Biometals 12:295–300

    Article  PubMed  CAS  Google Scholar 

  12. De Freitas JM, Liba A, Meneghini R, Valentine JS, Gralla EB (2000) Yeast lacking Cu–Zn superoxide dismutase show altered iron homeostasis. Role of oxidative stress in iron metabolism. J Biol Chem 275:11645–11649

    Article  PubMed  Google Scholar 

  13. Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Biol 201:1203–1209

    PubMed  CAS  Google Scholar 

  14. Hsu PC, Yang CY, Lan CY (2011) Candida albicans Hap43 is a repressor induced under low-iron conditions and is essential for iron-responsive transcriptional regulation and virulence. Eukaryot Cell 10:207–225

    Article  PubMed  CAS  Google Scholar 

  15. Hwang CS, Baek YU, Yim HS, Kang SO (2003) Protective roles of mitochondrial manganese-containing superoxide dismutase against various stresses in Candida albicans. Yeast 20:929–941

    Article  PubMed  CAS  Google Scholar 

  16. Hwang CS, Rhie GE, Kim ST et al (1999) Copper- and zinc-containing superoxide dismutase and its gene from Candida albicans. Biochim Biophys Acta 1427:245–255

    Article  PubMed  CAS  Google Scholar 

  17. Hwang CS, Rhie GE, Oh JH et al (2002) Copper- and zinc-containing superoxide dismutase is required for the protection from oxidative stresses and full virulence in Candida albicans. Microbiology 148:3705–3713

    PubMed  CAS  Google Scholar 

  18. Irazusta V, Moreno-Cermeno A, Cabiscol E, Ros J, Tamarit J (2008) Major targets of iron-induced protein oxidative damage in frataxin-deficient yeasts are magnesium-binding proteins. Free Radic Biol Med 44:1712–1723

    Article  PubMed  CAS  Google Scholar 

  19. Jensen LT, Cizewski-Culotta V (2000) Role of Saccharomyces cerevisiae ISA1 and ISA2 in iron homeostasis. Mol Cell Biol 20:3918–3927

    Article  PubMed  CAS  Google Scholar 

  20. Kang HA, Jung MS, Hong WK et al (1998) Expression and secretion of human serum albumin in the yeast Saccharomyces cerevisiae. J Microbiol Biotechnol 8:42–48

    CAS  Google Scholar 

  21. Lamarre C, Le May JD, Deslauriers N, Bourbonnais Y (2001) Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) up on the entry and during the stationary phase. J Biol Chem 276:43784–43791

    Article  PubMed  CAS  Google Scholar 

  22. Lenz AG, Costabel U, Shaltiel S, Levine RL (1989) Determination of carbonyl groups in oxidatively modified proteins by reduction with tritiated sodium borohydride. Anal Biochem 177:419–425

    Article  PubMed  CAS  Google Scholar 

  23. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagents. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  24. Martchenko M, Alarco AM, Harcus D, Whiteway M (2004) Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 15:456–467

    Article  PubMed  CAS  Google Scholar 

  25. Meneghini R (1997) Iron homeostasis, oxidative stress, and DNA damage. Free Radic Biol Med 23:783–792

    Article  PubMed  CAS  Google Scholar 

  26. O’Brien KM, Dirmeier R, Engle M, Poyton RO (2004) Mitochondrial protein oxidation in yeast mutants lacking manganese-(MnSOD) or copper- and zinc-containing superoxide dismutase (CuZnSOD): evidence that MnSOD and CuZnSOD have both unique and overlapping functions in protecting mitochondrial proteins from oxidative damage. J Biol Chem 279:51817–51827

    Article  PubMed  Google Scholar 

  27. Protchenko OV, Boretsky YR, Romanyuk TM, Fedorovych DV (2000) Oversynthesis of riboflavin by yeast Pichia guilliermondii in response to oxidative stress. Ukr Biokhim J 72:19–23

    CAS  Google Scholar 

  28. Raychaudhuri S, Reddy MM, Rajkumar NR, Rajasekharan R (2003) Cytosolic iron superoxide dismutase is a part of the triacylglycerol biosynthetic complex in oleaginous yeast. Biochem J 372:587–594

    Article  PubMed  CAS  Google Scholar 

  29. Rhie GE, Hwang CS, Brady MJ et al (1999) Manganese-containing superoxide dismutase and its gene from Candida albicans. Biochim Biophys Acta 1426:409–419

    Article  PubMed  CAS  Google Scholar 

  30. Rutherford JC, Ojeda L, Balk J et al (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J Biol Chem 280:10135–10140

    Article  PubMed  CAS  Google Scholar 

  31. Shavlovsky GM, Fedorovich DV, Babyak LY (1993) The effect of rib81 mutation on riboflavin biosynthesis and iron transport in yeast Pichia guilliermonlii yeast. Mikrobiologiya 62:897–903 (in Russian)

    Google Scholar 

  32. Shavlovsky GM, Fedorovich DV, Kutsiaba VI, Babyak LY, Stenchuk MM (1992) Participation of RIB80 gene in regulation of riboflavin biosynthesis and iron transport in yeast Pichia guilliermonlii. Genetika 28:25–32 (in Russian)

    Google Scholar 

  33. Shavlovsky GM, Koltun LV, Kshanovskaya BV, Logvinenko EM, Stenchuk NN (1989) Regulation of biosynthesis of riboflavin by elements of the positive control in Pichia guilliermonlii yeast. Genetika 25:250–258 (in Russian)

    Google Scholar 

  34. Spevak W, Fessl F, Rytka J, Ruis H et al (1983) Isolation of the catalase T structural gene of Saccharomyces cerevisiae by functional complementation. Mol Cell Biol 3:1545–1551

    PubMed  CAS  Google Scholar 

  35. Stadler JA, Schweyen RJ (2002) The yeast iron regulon is induced upon cobalt stress and crucial for cobalt tolerance. J Biol Chem 277:39649–39654

    Article  PubMed  CAS  Google Scholar 

  36. Temple MD, Perrone GG, Dawes IW (2005) Complex cellular responses to reactive oxygen species. Trends Cell Biol 15:319–326

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Analytical Biotechnology, Institute of Cell Biology NAS of Ukraine, Drahomanov Str. 14/16, Lviv, 79005, Ukraine

    Tetyana M. Prokopiv

  2. Department of Molecular Genetics and Biotechnology, Institute of Cell Biology NAS of Ukraine, Drahomanov Str. 14/16, Lviv, 79005, Ukraine

    Dariya V. Fedorovych, Yuriy R. Boretsky & Andriy A. Sibirny

  3. Department of Metabolic Engineering, Rzeszόw University, Ćwiklińskiej 2, 35-601, Rzeszow, Poland

    Andriy A. Sibirny

Authors
  1. Tetyana M. Prokopiv
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  2. Dariya V. Fedorovych
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  3. Yuriy R. Boretsky
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  4. Andriy A. Sibirny
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Correspondence to Andriy A. Sibirny.

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Prokopiv, T.M., Fedorovych, D.V., Boretsky, Y.R. et al. Oversynthesis of Riboflavin in the Yeast Pichia guilliermondii is Accompanied by Reduced Catalase and Superoxide Dismutases Activities. Curr Microbiol 66, 79–87 (2013). https://doi.org/10.1007/s00284-012-0242-0

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