Zymogram profiling of superoxide dismutase and catalase activities allows Saccharomyces and non-Saccharomyces species differentiation and correlates to their fermentation performance

Applied Microbiology and Biotechnology

Volumn 97, Issue 10, 2013, Pages 4563-4576

  Gamero Sandemetrio, Esther ^a   Gómez Pastor, Rocío ^b   Matallana, Emilia ^a,b  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

Catalase; Fermentative capacity; Superoxide dismutase; Yeast; Zymogram

Indexed keywords

CATALASE; CATALASE ENZYME ACTIVITIES; ENZYMATIC AND NON-ENZYMATIC ANTIOXIDANTS; FERMENTATION PERFORMANCE; FERMENTATIVE CAPACITY; SPECIES DIFFERENTIATIONS; SUPER OXIDE DISMUTASE; ZYMOGRAM;

OXYGEN; PEPTIDES;

YEAST;

CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE;

ANTIOXIDANT; BIOCHEMISTRY; BIOTECHNOLOGY; DETECTION METHOD; ENZYME ACTIVITY; FERMENTATION; FUNCTIONAL ROLE; IDENTIFICATION METHOD; METABOLISM; METABOLITE; MICROBIAL ACTIVITY; OXIC CONDITIONS; PROTEIN; YEAST;

ANTIOXIDANT ACTIVITY; ARTICLE; CANDIDA ALBICANS; CANDIDA STELLATA; ENZYME ACTIVITY; FERMENTATION; HANSENIOSPORA GUILLIERMONDII; HANSENIOSPORA OSMOPHILA; IMMERSION; NONHUMAN; PICHIA; PICHIA FERMENTANS; PICHIA PASTORIS; SACCHAROMYCES; SACCHAROMYCES BAYANUS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES KUDRIAVZEVII; SACCHAROMYCES PARADOXUS; SEQUENCE ALIGNMENT; TORULASPORA; ZYMOGRAPHY;

BIOMASS; CATALASE; CELL DIFFERENTIATION; FERMENTATION; SACCHAROMYCES; SUPEROXIDE DISMUTASE;

SACCHAROMYCES;

EID: 84877745339     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4672-1     Document Type: Article

References (49)

1. Aksam EB, De Vries B, Van Der Klei IJ, Kiel JAKW (2009) Preserving organelle vitality: peroxisomal quality control mechanisms in yeast. FEMS Yeast Res 9:808-820
2. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276-287
3. Borders CL, Saunders JE, Blech DM, Fridovich I (1985) Essentiality of the active-site arginine residue for the normal catalytic activity of Cu, Zn superoxide dismutase. Arch Biochem Biophys 241:472-476 (Pubitemid 15023276)
4. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248-254
5. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, Valentine JS, Culotta VC (2004) Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc Natl Acad Sci 101:5964-5969 (Pubitemid 38520511)
6. Cohen G, Rapatz W, Ruis H (1988) Sequence of the Saccharomyces cerevisiae CTA1 gene and amino acid sequence of catalase A derived from it. Eur J Biochem 176:159-163
7. Dellomonaco C, Amaretti A, Zanoni S, Pompei A, Matteuzzi D, Rossi M (2007) Fermentative production of superoxide dismutase with Kluyveromyces marxianus. J Ind Microbiol Biotechnol 34:27-34 (Pubitemid 44951528)
8. Fridovich I (1978) Superoxide dismutases: defence against endogenous superoxide radical. Ciba Found Symp 65:77-93
9. Fridovich I (1995) Superoxide radical and superoxide dismutase. Annu Rev Biochem 64:97-112
10. Fridovich I (2011) Superoxide dismutase: anti- versus pro- oxidants? Anticancer Agents Med Chem 11:175-177
11. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241-4257
12. Gomez-Pastor R, Perez-Torrado R, Cabiscol E, Ros J, Matallana E (2010) Reduction of oxidative cellular damage by overexpression of the thioredoxin TRX2 gene improves yield and quality of wine yeast dry active biomass. Microb Cell Fact 9:9
13. Gregory EM, Goscin SA, Fridovich I (1974) Superoxide dismutase and oxygen toxicity in a eukaryote. J Bacteriol 2:456-460
14. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vynilpyridine. Anal Biochem 106:207-212 (Pubitemid 11246585)
15. Iqbal J, Whitney P (1991) Use of cyanide and diethyldithiocarbamate in the assay of superoxide dismutases. Free Radic Biol Med 10:69-77 (Pubitemid 121003213)
16. Jakubowski W, Bilinski T, Bartosz G (2000) Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. Free Radic Biol Med 28:659-664 (Pubitemid 30171278)
17. Kuthan H, Haussmann HJ, Werringloer J (1986) A spectrophotometric assay for superoxide dismutase activities in crude tissue fractions. Biochem J 237:175-180 (Pubitemid 16063104)
18. Lamarre C, LeMay JD, Deslauriers N, Bourbonnais Y (2001) Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J Biol Chem 276:43784-43791
19. Lamb AL, Torres AS, O'Halloran TV, Rosenzweig AC (2001) Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat Struct Biol 8:751-755 (Pubitemid 32803590)
20. Landolfo S, Politi H, Angelozzi D, Mannazzu I (2008) ROS accumulation and oxidative damage to cell structures in Saccharomyces cerevisiae wine strains during fermentation of high-sugar-containing medium. Biochim Biophys Acta 6:892-898
21. Landolfo S, Zara G, Zara S, Budroni M, Ciani M, Mannazzu I (2010) Oleic acid and ergosterol supplementation mitigates oxidative stress in wine strains of Saccharomyces cerevisiae. Int J Food Microbiol 141:229-35
22. 2 formation. Free Radic Biol Med 42:1465-1469 (Pubitemid 46590616)
23. Luk EE, Culotta VC (2001) Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J Biol Chem 276:47556-47562
24. Luk EE, Yang M, Jensen LT, Bourbonnais Y, Culotta VC (2005) Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J Biol Chem 280:22715-22720 (Pubitemid 40853176)
25. Lushchak V, Semchyshyn H, Lushchak O, Mandryk S (2005) Diethyldithiocarbamate inhibits in vivo Cu, Zn-superoxide dismutase and perturbs free radical processes in the yeast Saccharomyces cerevisiae cells. Biochem Biophys Res Commun 338:1739-1744 (Pubitemid 41643084)
26. Mannarino SC, Vilela LF, Brasil AA, Aranha JN, Moradas-Ferreira P, Pereira MD, Costa V, Eleutherio EC (2011) Requirement of glutathione for Sod1 activation during lifespan extension. Yeast 28:19-25
27. Mannervik B (1987) The enzymes of glutathione metabolism: an overview. Biochem Soc Trans 15:717-718
28. Misra HP, Fridovich I (1972) The purification and properties of superoxide dismutase from Neurospora crassa. J Biol Chem 247:3410-3414
29. Moradas-Ferreira P, Costa V, Piper P, Mager W (1996) The molecular defences against reactive oxygen species in yeast. Mol Microbiol 19:651-658 (Pubitemid 26068582)
30. Nagi MN, al-Bekairi AM, al-Sawaf HA (1995) Spectrophotometric assay for superoxide dismutase based on the nitroblue tetrazolium reduction by glucose-glucose oxidase. Biochem. Mol Biol Int 36:633-638 (Pubitemid 26173022)
31. Nishida O, Kuwazaki S, Suzuki C, Shima J (2004) Superior molasses assimilation, stress tolerance, and trehalose accumulation of baker's yeast isolated from dried sweet potatoes (hoshi-imo). Biosci Biotechnol Biochem 68:1442-1448 (Pubitemid 40059206)
32. Parrou JL, Frrancois J (1997) A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal Biochem 248:186-188 (Pubitemid 27218240)
33. Penninckx MJ (2002) An overview on glutathione in Saccharomyces versus non-conventional yeasts. FEMS Yeast Res 2:295-305
34. Pernin P, Grelaud G (1989) Application of isoenzymatic typing to the identification of nonaxenic strains of Naegleria (Protozoa, Rizopoda). Parasitol Res 75:595-598 (Pubitemid 19205858)
35. Querol A, Barrio E, Huerta T, Ramon D (1992) Molecular monitoring of wine fermentations conducted by active dry yeast strains. Appl Environ Microbiol 58:2948-2953
36. Raimondi S, Uccelletti D, Matteuzzi D, Pagnoni UM, Rossi M, Palleschi C (2008) Characterization of the superoxide dismutase SOD1 gene of Kluyveromyces marxianus L3 and improved production of SOD activity. Appl Microbiol Biotechnol 77:1269-1277
37. Reddy CD, Venkaiah B (1984) Purification and characterization of Cu-Zn superoxide dismutase from mungbean (Vigna radiata) seedlings. J Biosci 6:115-123
38. Rainieri S, Zambonelli C, Kaneko Y (2003) Saccharomyces sensu stricto: systematic, genetic diversity and evolution. J Biosci Bioeng 96:1-9 (Pubitemid 37026296)
39. Rodriguez-Porrata B, Novo M, Guillamon J, Rozes N, Mas A, Otero RC (2008) Vitality enhancement of the rehydrated active dry wine yeast. Int J Food Microbiol 126:116-122
40. Schmidt PJ, Ramos-Gomez M, Culotta VC (1999) A gain of superoxide dismutase (SOD) activity obtained with CCS, the copper metallochaperone for SOD1. J Biol Chem 274:36952-36956 (Pubitemid 30016763)
41. Shukla MR, Yadav R, Desai A (2009) Catalase and superoxide dismutase double staining zymogram technique for Deinococcus and Kocuria species exposed to multiple stresses. J Basic Microbiol 49:593-597
42. Soung N, Lee Y (2000) Iso-catalase profiles of Deinococcus spp. J Biochem Mol Biol 33:412-416
43. Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC (2001) A fraction of yeast Cu, Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria. A physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276:38084-38089
44. Vianna CR, Silva CL, Neves MJ, Rosa CA (2008) Saccharomyces cerevisiae strains from traditional fermentations of Brazilian cachaca: trehalose metabolism, heat and ethanol resistance. Antonie van Leeuwenhoek 93:205-217
45. Wayne LG, Diaz GA (1986) A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels. Anal Biochem 157:89-92
46. Weisinger RA, Fridovich I (1973) Mitochondrial superoxide dismutase. J Biol Chem 248:4793-4796
47. Yun EJ, Lee YN (2000) Production of two different catalase-peroxidases by Deinococcus radiophilus. FEMS Microbiol Lett 184:155-159 (Pubitemid 30125333)
48. Zhou W, Ryan JJ, Zhou H (2004) Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses. J Biol Chem 279:32262-32268 (Pubitemid 39014675)
49. Zuzuarregui A, Monteoliva L, Gil C, del Olmo M (2006) Transcriptomica and proteomic approach for understanding the molecular basis of adaptation of Saccharomyces cerevisiae to wine fermentation. Appl Environ Microbiol 72:836-47