1887

Abstract

Cold-induced oxidative stress during the aging of three strains (two Antarctic and one from a temperate region) in stationary culture was documented and demonstrated a significant increase in the protein carbonyl content, the accumulation of glycogen and trehalose, and an increase in the activities of antioxidant enzymes (superoxide dismutase and catalase). The cell response to a temperature downshift depends on the degree of stress and the temperature characteristics of the strains. Our data give further support for the role of oxidative stress in the aging of fungi in stationary cultures. Comparing the present results for the stationary growth phase with our previous results for the exponential growth phase was informative concerning the relationship between the cold-stress response and age-related changes in the tested strains. Unlike the young cells, stationary-phase cultures demonstrated a more pronounced level of oxidative damage, as well as decreased antioxidant defence.

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2017-07-01
2024-03-28
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References

  1. Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012; 2012:1–26 [View Article]
    [Google Scholar]
  2. Borges AA, Jiménez-Arias D, Expósito-Rodríguez M, Sandalio LM, Pérez JA. Priming crops against biotic and abiotic stresses: MSB as a tool for studying mechanisms. Front Plant Sci 2014; 5:642 [View Article][PubMed]
    [Google Scholar]
  3. Cupul WC, Abarca GH, Vázquez RR, Salmones D, Hernández RG et al. Response of ligninolytic macrofungi to the herbicide atrazine: dose-response bioassays. Rev Argent Microbiol 2014; 46:348–357 [View Article][PubMed]
    [Google Scholar]
  4. Halliwell B. Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 2006; 141:312–322 [View Article][PubMed]
    [Google Scholar]
  5. Bai Z, Harvey LM, Mcneil B. Oxidative stress in submerged cultures of fungi. Crit Rev Biotechnol 2003; 23:267–302 [View Article][PubMed]
    [Google Scholar]
  6. Bertram C, Hass R. Cellular responses to reactive oxygen species-induced DNA damage and aging. Biol Chem 2008; 389:211–220 [View Article][PubMed]
    [Google Scholar]
  7. Fridovich I. Oxygen toxicity: a radical explanation. J Exp Biol 1998; 201:1203–1209[PubMed]
    [Google Scholar]
  8. Angelova MB, Pashova SB, Spasova BK, Vassilev SV, Slokoska LS. Oxidative stress response of filamentous fungi induced by hydrogen peroxide and paraquat. Mycol Res 2005; 109:150–158 [View Article][PubMed]
    [Google Scholar]
  9. Castro FA, Herdeiro RS, Panek AD, Eleutherio EC, Pereira MD. Menadione stress in Saccharomyces cerevisiae strains deficient in the glutathione transferases. Biochim Biophys Acta 2007; 1770:213–220 [View Article][PubMed]
    [Google Scholar]
  10. Skyba M, Petijová L, Košuth J, Koleva DP, Ganeva TG et al. Oxidative stress and antioxidant response in Hypericum perforatum L. plants subjected to low temperature treatment. J Plant Physiol 2012; 169:955–964 [View Article][PubMed]
    [Google Scholar]
  11. Chattopadhyay MK, Raghu G, Sharma YV, Biju AR, Rajasekharan MV et al. Increase in oxidative stress at low temperature in an Antarctic bacterium. Curr Microbiol 2011; 62:544–546 [View Article][PubMed]
    [Google Scholar]
  12. Lushchak VI. Adaptive response to oxidative stress: bacteria, fungi, plants and animals. Comp Biochem Physiol C Toxicol Pharmacol 2011; 153:175–190 [View Article][PubMed]
    [Google Scholar]
  13. Awasthi R, Bhandari K, Nayyar H. Temperature stress and redox homeostasis in agricultural crops. Front Environ Sci 2015; 3:11 [View Article]
    [Google Scholar]
  14. Lukatkin AS. Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: 2. The activity of antioxidant enzymes during plant chilling. Russ J Plant Physiol 2002; 49:782–788 [View Article]
    [Google Scholar]
  15. Yang H, Wu F, Cheng J. Reduced chilling injury in cucumber by nitric oxide and the antioxidant response. Food Chem 2011; 127:1237–1242 [View Article][PubMed]
    [Google Scholar]
  16. Sahoo DD, Kara TC. Cold stress-induced lipid peroxidation and non-enzymatic antioxidant defense in tissues of the common Indian toad, Bufo melanostictus. Arch Biol Sci 2014; 66:1303–1310 [View Article]
    [Google Scholar]
  17. Smirnova GV, Zakirova ON, Oktyabrskii ON. The role of antioxidant systems in the cold stress response of Escherichia coli. Microbiology 2001; 70:45–50 [View Article]
    [Google Scholar]
  18. Soto T, Beltrán FF, Paredes V, Madrid M, Millar JB et al. Cold induces stress-activated protein kinase-mediated response in the fission yeast Schizosaccharomyces pombe. Eur J Biochem 2002; 269:5056–5065 [View Article][PubMed]
    [Google Scholar]
  19. Hayashi M, Maeda T. Activation of the HOG pathway upon cold stress in Saccharomyces cerevisiae. J Biochem 2006; 139:797–803 [View Article][PubMed]
    [Google Scholar]
  20. Zakharova K, Marzban G, de Vera JP, Lorek A, Sterflinger K. Protein patterns of black fungi under simulated Mars-like conditions. Sci Rep 2014; 4:5114 [View Article][PubMed]
    [Google Scholar]
  21. Gocheva YG, Krumova ET, Slokoska LS, Miteva JG, Vassilev SV et al. Cell response of Antarctic and temperate strains of Penicillium spp. to different growth temperature. Mycol Res 2006; 110:1347–1354 [View Article][PubMed]
    [Google Scholar]
  22. Gocheva YG, Tosi S, Krumova ET, Slokoska LS, Miteva JG et al. Temperature downshift induces antioxidant response in fungi isolated from Antarctica. Extremophiles 2009; 13:273–281 [View Article][PubMed]
    [Google Scholar]
  23. Tosi S, Kostadinova N, Krumova E, Pashova S, Dishliiska V et al. Antioxidant enzyme activity of filamentous fungi isolated from Livingston Island, Maritime Antarctica. Polar Biol 2010; 33:1227–1237 [View Article]
    [Google Scholar]
  24. Kostadinova N, Krumova E, Stefanova T, Dishliyska V, Angelova M et al. Transient cold shock induces oxidative stress events in Antarctic fungi. In Lushchak VI, Stoliar O. (editors) Oxidative Stress Rijeka, Croatia: InTech; 2012 pp. 75–99
    [Google Scholar]
  25. Sena LA, Chandel NS. Physiological roles of mitochondrial reactive oxygen species. Mol Cell 2012; 48:158–167 [View Article][PubMed]
    [Google Scholar]
  26. Malinin NL, West XZ, Byzova TV. Oxidation as "the stress of life". Aging 2011; 3:906–910 [View Article][PubMed]
    [Google Scholar]
  27. Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956; 11:298–300 [View Article][PubMed]
    [Google Scholar]
  28. Sohal RS, Orr WC. Relationship between antioxidants, prooxidants, and the aging process. Ann N Y Acad Sci 1992; 663:74–84 [View Article][PubMed]
    [Google Scholar]
  29. Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996; 273:59–63 [View Article][PubMed]
    [Google Scholar]
  30. Muller FL, Lustgarten MS, Jang Y, Richardson A, van Remmen H. Trends in oxidative aging theories. Free Radic Biol Med 2007; 43:477–503 [View Article][PubMed]
    [Google Scholar]
  31. Osiewacz H. Aging and longevity in the filamentous fungus Podospora anserina. In Osiewacz HD. (editor) Aging of Organisms Rijeka, Croatia: Kluwer Academic Publishers; 2003 pp. 31–53 [CrossRef]
    [Google Scholar]
  32. Miteva-Staleva J, Stefanova T, Krumova E, Angelova M. Growth-phase-related changes in reactive oxygen species generation as a cold stress response in Antarctic Penicillium strains. Biotechnol Biotechnol Equip 2011; 25:58–63 [View Article]
    [Google Scholar]
  33. Miteva-Staleva J, Krumova E, Stefanova T, Angelova M. Age-related changes in reactive oxygen species production in the filamentous fungus Penicillium rugulosum T35 under cold stress conditions. C R Acad Bulg Sci 2015; 68:1123–1128
    [Google Scholar]
  34. Owsiak A, Bartosz G, Bilinski T. Oxidative stress during aging of the yeast in a stationary culture and its attenuation by antioxidants. Cell Biol Int 2010; 34:731–736 [View Article][PubMed]
    [Google Scholar]
  35. Beauchamp C, Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 1971; 44:276–287 [View Article][PubMed]
    [Google Scholar]
  36. Beers RF, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 1952; 195:133–140[PubMed]
    [Google Scholar]
  37. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193:265–275[PubMed]
    [Google Scholar]
  38. Becker JU. A method for glycogen determination in whole yeast cells. Anal Biochem 1978; 86:56–64 [View Article][PubMed]
    [Google Scholar]
  39. Vandercammen A, François JM, Torres BB, Maia JC, Hers HG. Fructose 2,6-bisphosphate and carbohydrate metabolism during the life cycle of the aquatic fungus Blastocladiella emersonii. J Gen Microbiol 1990; 136:137–146 [View Article][PubMed]
    [Google Scholar]
  40. Parrou JL, Teste MA, François J. Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology 1997; 143:1891–1900 [View Article][PubMed]
    [Google Scholar]
  41. Somogyi M. Notes on sugar determination. J Biol Chem 1952; 195:19–23[PubMed]
    [Google Scholar]
  42. Hart PJ, Balbirnie MM, Ogihara NL, Nersissian AM, Weiss MS et al. A structure-based mechanism for copper-zinc superoxide dismutase. Biochemistry 1999; 38:2167–2178 [View Article][PubMed]
    [Google Scholar]
  43. Adachi H, Ishii N. Effects of tocotrienols on life span and protein carbonylation in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 2000; 55:B280–B285 [View Article][PubMed]
    [Google Scholar]
  44. Hagen TM. Oxidative stress, redox imbalance, and the aging process. Antioxid Redox Signal 2003; 5:503–506 [View Article][PubMed]
    [Google Scholar]
  45. Gladyshev VN. The free radical theory of aging is dead. Long Live the Damage Theory!. Antioxid Redox Signal 2014; 20:727–731 [CrossRef]
    [Google Scholar]
  46. Buzzini P, Margesin R. Cold-adapted yeasts: a lesson from the cold and a challenge for the XXI century. In Buzzini P, Margesin R. (editors) Cold-Adapted Yeasts: Biodiversity, Adaptation Strategies and Biotechnological Significance Berlin: Springer-Verlag; 2014 pp. 3–22 [CrossRef]
    [Google Scholar]
  47. Alcaíno J, Cifuentes V, Baeza M. Physiological adaptations of yeasts living in cold environments and their potential applications. World J Microbiol Biotechnol 2015; 31:1467–1473 [View Article][PubMed]
    [Google Scholar]
  48. Yamanaka K, Araki J, Takano M, Sekiguchi J. Characterization of Bacillus subtilis mutants resistant to cold shock-induced autolysis. FEMS Microbiol Lett 1997; 150:269–275 [View Article][PubMed]
    [Google Scholar]
  49. Nevarez L, Vasseur V, Le Dréan G, Tanguy A, Guisle-Marsollier I et al. Isolation and analysis of differentially expressed genes in Penicillium glabrum subjected to thermal stress. Microbiology 2008; 154:3752–3765 [CrossRef]
    [Google Scholar]
  50. Nevarez L, Vasseur V, Debaets S, Barbier G. Use of response surface methodology to optimise environmental stress conditions on Penicillium glabrum, a food spoilage mould. Fungal Biol 2010; 114:490–497 [View Article][PubMed]
    [Google Scholar]
  51. Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S. Fungi in Antarctica. Rev Environ Sci Biotechnol 2007; 6:127–141 [View Article]
    [Google Scholar]
  52. Newsham KK, Upson R, Read DJ. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2009; 2:10–20 [View Article]
    [Google Scholar]
  53. Fenice M. The psychrotolerant Antarctic fungus Lecanicillium muscarium CCFEE 5003: a powerful producer of cold-tolerant chitinolytic enzymes. Molecules 2016; 21:447 [View Article][PubMed]
    [Google Scholar]
  54. Hébraud M, Potier P. Cold shock response and low temperature adaptation in psychrotrophic bacteria. J Mol Microbiol Biotechnol 1999; 1:211–219[PubMed]
    [Google Scholar]
  55. Sámi L. The role of chitinolytic enzymes and free radicals in the autolysis of Penicillium chrysogenum. PhD thesis, University of Debrecen 2003
  56. Mcneil B, Berry DR, Harvey LM, Grant A, White S. Measurement of autolysis in submerged batch cultures of Penicillium chrysogenum. Biotechnol Bioeng 1998; 57:297–305 [View Article][PubMed]
    [Google Scholar]
  57. Zalar P, Gunde-Cimerman N. Cold-adapted yeasts in Arctic habitats. In Buzzini P, Margesin R. (editors) Cold-Adapted Yeasts: Biodiversity, Adaptation Strategies and Biotechnological Significance Berlin: Springer-Verlag; 2014 pp. 49–74 [CrossRef]
    [Google Scholar]
  58. Hassan N, Rafiq M, Hayat M, Shah AA, Hasan F. Psychrophilic and psychrotrophic fungi: a comprehensive review. Rev Environ Sci Biotechnol 2016; 15:147–172 [View Article]
    [Google Scholar]
  59. Friguet B. Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett 2006; 580:2910–2916 [View Article][PubMed]
    [Google Scholar]
  60. Pena LB, Azpilicueta CE, Benavides MP, Gallego SM. Protein oxidative modifications. In Gupta DK, Sandalio LM. (editors) Metal Toxicity in Plants: Perception, Signaling and Remediation Berlin: Springer Verlag; 2012 pp. 207–225 [CrossRef]
    [Google Scholar]
  61. Suzuki N, Mittler R. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 2006; 126:45–51 [View Article]
    [Google Scholar]
  62. Belinky PA, Flikshtein N, Lechenko S, Gepstein S, Dosoretz CG. Reactive oxygen species and induction of lignin peroxidase in Phanerochaete chrysosporium. Appl Environ Microbiol 2003; 69:6500–6506 [View Article][PubMed]
    [Google Scholar]
  63. Li Q, Harvey LM, Mcneil B. The effects of elevated process temperature on the protein carbonyls in the filamentous fungus, Aspergillus niger B1-D. Process Biochem 2008; 43:877–881 [View Article]
    [Google Scholar]
  64. Krumova EZ, Pashova SB, Dolashka-Angelova PA, Stefanova T, Angelova MB. Biomarkers of oxidative stress in the fungal strain Humicola lutea under copper exposure. Process Biochem 2009; 44:288–295 [View Article]
    [Google Scholar]
  65. Stadtman ER. Protein oxidation and aging. Free Radic Res 2006; 40:1250–1258 [View Article][PubMed]
    [Google Scholar]
  66. Reverter-Branchat G, Cabiscol E, Tamarit J, Ros J. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae: common targets and prevention by calorie restriction. J Biol Chem 2004; 279:31983–31989 [View Article][PubMed]
    [Google Scholar]
  67. Fu XH, Meng FL, Hu Y, Zhou JQ. Candida albicans, a distinctive fungal model for cellular aging study. Aging Cell 2008; 7:746–757 [View Article][PubMed]
    [Google Scholar]
  68. de Castro C, del Valle P, Rúa J, García-Armesto MR, Gutiérrez-Larraínzar M et al. Antioxidant defence system during exponential and stationary growth phases of Phycomyces blakesleeanus: response to oxidative stress by hydrogen peroxide. Fungal Biol 2013; 117:275–287 [View Article][PubMed]
    [Google Scholar]
  69. Schade B, Jansen G, Whiteway M, Entian KD, Thomas DY. Cold adaptation in budding yeast. Mol Biol Cell 2004; 15:5492–5502 [View Article][PubMed]
    [Google Scholar]
  70. Dalmasso M, Aubert J, Even S, Falentin H, Maillard MB et al. Accumulation of intracellular glycogen and trehalose by Propionibacterium freudenreichii under conditions mimicking cheese ripening in the cold. Appl Environ Microbiol 2012; 78:6357–6364 [View Article][PubMed]
    [Google Scholar]
  71. Abrashev RI, Pashova SB, Stefanova LN, Vassilev SV, Dolashka-Angelova PA et al. Heat-shock-induced oxidative stress and antioxidant response in Aspergillus niger 26. Can J Microbiol 2008; 54:977–983 [View Article][PubMed]
    [Google Scholar]
  72. François J, Parrou JL. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 2001; 25:125–145 [View Article][PubMed]
    [Google Scholar]
  73. Lazarova N, Krumova E, Stefanova T, Georgieva N, Angelova M. The oxidative stress response of the filamentous yeast Trichosporon cutaneum R57 to copper, cadmium and chromium exposure. Biotechnol Biotechnol Equip 2014; 28:855–862 [View Article][PubMed]
    [Google Scholar]
  74. Bolat I. The importance of trehalose in brewing yeast survival. Innov Rom Food Biotechnol 2008; 2:1–10
    [Google Scholar]
  75. Roy A, Ghosh AK. Correlation between stationary phase survival and acid trehalase activity in yeast. Biochim Biophys Acta 1998; 1401:235–238 [View Article][PubMed]
    [Google Scholar]
  76. Hu J, Wei M, Mirzaei H, Madia F, Mirisola M et al. Tor-Sch9 deficiency activates catabolism of the ketone body-like acetic acid to promote trehalose accumulation and longevity. Aging Cell 2014; 13:457–467 [View Article][PubMed]
    [Google Scholar]
  77. Samokhvalov VA, Mel'nikov GV, Ignatov VV. Role of trehalose and glycogen in the survival of aging Saccharomyces cerevisiae cells. Mikrobiologiia 2004; 73:449–454 [View Article]
    [Google Scholar]
  78. Longo VD, Gralla EB, Valentine JS. Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 1996; 271:12275–12280 [View Article][PubMed]
    [Google Scholar]
  79. Cuéllar-Cruz M, Briones-Martin-del-Campo M, Cañas-Villamar I, Montalvo-Arredondo J, Riego-Ruiz L et al. High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot Cell 2008; 7:814–825 [View Article][PubMed]
    [Google Scholar]
  80. Li Q, Harvey LM, Mcneil B. Oxidative stress in industrial fungi. Crit Rev Biotechnol 2009; 29:199–213 [View Article][PubMed]
    [Google Scholar]
  81. Takagi H, Shima J. Stress tolerance of baker’s yeast during bread-making. In Takagi H, Kitagaki H. (editors) Stress Biology of Yeasts and Fungi Tokyo: Springer; 2015 pp. 23–42 [CrossRef]
    [Google Scholar]
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