Skip to main content
Log in

Temperature downshift induces antioxidant response in fungi isolated from Antarctica

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Although investigators have been studying the cold-shock response in a variety of organisms for the last two decades or more, comparatively little is known about the difference between antioxidant cell response to cold stress in Antarctic and temperate microorganisms. The change of environmental temperature, which is one of the most common stresses, could be crucial for their use in the biotechnological industry and in ecological research. We compared the effect of short-term temperature downshift on antioxidant cell response in Antarctic and temperate fungi belonging to the genus Penicillium. Our study showed that downshift from an optimal temperature to 15° or 6°C led to a cell response typical of oxidative stress: significant reduction of biomass production; increase in the levels of oxidative damaged proteins and accumulation of storage carbohydrates (glycogen and trehalose) in comparison to growth at optimal temperature. Cell response against cold stress includes also increase in the activities of SOD and CAT, which are key enzymes for directly scavenging reactive oxygen species. This response is more species-dependent than dependent on the degree of cold-shock. Antarctic psychrotolerant strain Penicillium olsonii p14 that is adapted to life in extremely cold conditions demonstrated enhanced tolerance to temperature downshift in comparison with both mesophilic strains (Antarctic Penicillium waksmanii m12 and temperate Penicillium sp. t35).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

SOD:

Superoxide dismutase

CAT:

Catalase

ROS:

Reactive oxygen species

NBT:

Nitro-blue tetrazolium

DNPH:

2, 4-Dinitrophenylhydrazine

References

  • Abele D, Tesch C, Wencke P, Pörtner HO (2001) How do oxidative stress parameters relate to thermal tolerance in the Antarctic bivalve Yoldia eightsi? Antarctic Sci 13:111–118

    Article  Google Scholar 

  • Adachi H, Ishii N (2000) Effects of tocotrienols on life span and protein carbonylation in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 55:B280–B285

    PubMed  CAS  Google Scholar 

  • Angelova M, Genova L, Slokoska L, Pashova S (1995) Effect of glucose on the superoxide dismutase production in fungal strain Humicola lutea. Can J Microbiol 41:978–983

    Article  PubMed  CAS  Google Scholar 

  • Ansaldo M, Polo J, Evelson P, Luquet C, Llesuy S (2000) Antioxidant levels from different Antarctic fish caught around South Georgia Island and Shag Rocks. Polar Biol 23:160–165

    Article  Google Scholar 

  • Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238

    CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  PubMed  CAS  Google Scholar 

  • Becker JU (1978) A method of glycogen determination in whole yeast cells. Anal Biochem 86:56–64

    Article  PubMed  CAS  Google Scholar 

  • Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogene peroxide by catalase. J Biol Chem 195:133–140

    PubMed  CAS  Google Scholar 

  • Cavicchioli R, Thomas T, Curmi PMG (2000) Cold stress response in Archaea. Extremophiles 4:321–331

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhyay MK (2002) Low temperature and oxidative stress. Curr Sci 83:109

    Google Scholar 

  • Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31:157–165

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61

    Article  CAS  Google Scholar 

  • Collén J, Davison IR (2001) Seasonality and thermal acclimation of reactive oxygen metabolism in Fucus vesiculosus (Phaeophyceae). J Phycol 37:474–481

    Article  Google Scholar 

  • Davies KJA, Goldberg AL (1987) Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells. J Biol Chem 262:8227–8234

    PubMed  CAS  Google Scholar 

  • Deegenaars ML, Watson K (1998) Heat shock response in the thermophilic enteric yeast Arxiozyma telluris. Appl Environ Microbiol 64:3063–3065

    PubMed  CAS  Google Scholar 

  • Gocheva Y, Krumova E, Slokoska L, Gesheva V, Angelova M (2005) Isolation of filamentous fungi from Antarctica. C R Acad Bulg Sci 58:403–408

    Google Scholar 

  • Gocheva Y, Krumova E, Slokoska L, Miteva J, Angelova M (2006) Cell response of Antarctic and temperate strains of Penicillium spp. to different growth temperature. Mycol Res 110:1347–1354

    Article  PubMed  CAS  Google Scholar 

  • Guderley H (2004) Metabolic responses to low temperature in fish muscle. Biol Rev 79:409–427

    Article  PubMed  Google Scholar 

  • Hart PJ, Belbirine MM, Ogihara NL, Nersissian AM, Weiss MS, Valentine JS, Eisenberg D (1999) A structure-based mechanism for cooper-zinc superoxide dismutase. Biochemistry 38:2167–2178

    Article  PubMed  CAS  Google Scholar 

  • Heise K, Puntarulo S, Nikinmaa M, Lucassen M, Pörtner H-O, Abele D (2006) Oxidative stress and HIF-1 DNA binding during stressful cold exposure and recovery in the North Sea eelpout (Zoarces viviparus). Comp Biochem Physiol 143:494–503

    Article  CAS  Google Scholar 

  • Kandror O, DeLeon A, Goldberg AL (2002) Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99:9727–9732

    Article  PubMed  CAS  Google Scholar 

  • Lowry OH, Rosenbrough HJ, Faar AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Michaud L, Di Cello F, Brilli M, Fani R, Lo Giudice A, Bruni V (2004) Biodiversity of cultivable psychrotrophic marine bacteria isolated from Terra Nova Bay (Ross Sea, Antarctica). FEMS Microbiol Lett 230:63–71

    Article  PubMed  CAS  Google Scholar 

  • Mizuno N, Sugie A, Kobayashi F, Takumi S (2008) Mitochondrial alternative pathway is associated with development of freezing tolerance in common wheat. J Plant Physiol 165:462–467

    Article  PubMed  CAS  Google Scholar 

  • Narinx E, Baise E, Gerday C (1997) Subtilisin from psychrophilic antarctic bacteria: characterization and site-directed mutagenesis of residues possibly involved in the adaptation to cold. Protein Eng 10:1271–1279

    Article  PubMed  CAS  Google Scholar 

  • Nichols DS, Sanderson K, Buia AD, Van de Kamp JL, Holloway PE, Bowman JP, Smith M, Mancuso-Nichols CA, Nichols PD, McMeekin TA (2002) Protein engineering, bioprospecting and biotechnology in Antarctica. In: Jabour-Green J, Haward M (eds) The Antarctic: past, present and future. Antarctic CRC Research Report #28, Hobart, pp 85–103

  • Ouellet F (2007) Cold acclimation and freezing tolerance in plants. Encyclopedia of life sciences, Wiley, London, pp 1–6

  • Parrou JL, Teste MA, Francois J (1997) 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 143:1891–1900

    Article  PubMed  CAS  Google Scholar 

  • Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol 114:1369–1376

    PubMed  CAS  Google Scholar 

  • Ray MK (2006) Cold-stress response of low temperature adapted bacteria. In: Sreedhar AS, Srinivas UK (eds) Stress response, A molecular biology approach, Research Signpost Kerala, India, pp 1–23

  • Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    Article  CAS  Google Scholar 

  • Rúa J, de Cima S, del Valle P, Gutiérrez-Larraínzar M, Busto F, de Arriaga D (2008) Glycogen and trehalose mobilization by acetic acid in Phycomyces blakesleeanus: dependence on the anion form. Res Microbiol 159:200–206

    Article  PubMed  CAS  Google Scholar 

  • Russell N (2006) Antarctic microorganisms: coming in from the cold. Culture (Oxoid) 27:1–4

    Google Scholar 

  • Sahara T, Goda T, Ohgiya S (2002) Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. J Biol Chem 277:50015–50021

    Article  PubMed  CAS  Google Scholar 

  • Şahin E, Gümüşlü S (2004) Cold-stress-induced modulation of antioxidant defense: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 48:165–171

    Article  PubMed  Google Scholar 

  • Selman C, Grune T, Al Stolzing, Jakstadt M, McLaren JS, Speakman JR (2002) The consequences of acute cold exposure on protein oxidation and proteasome activity in short-tailed field voles, Microtus agrestis. Free Radic Biol Med 33:259–265

    Article  PubMed  CAS  Google Scholar 

  • Sies H (1985) Oxidative stress. Introductory remarks. In: Sies H (ed) Academic Press, London, pp 1–8

  • Silljé HHW, Paalman JWG, Schure EG, Olsthoorn SQB, Verkleij AJ, Boonstra J, Verrips CT (1999) Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae. J Bacteriol 181:396–400

    PubMed  Google Scholar 

  • Smirnova GV, Zakirova ON, Oktyabrskii ON (2001) The role of antioxidant systems in the cold stress response of Escherichia coli. Microbiologia (Moskow) 70:45–50

    CAS  Google Scholar 

  • Somogy M (1952) Notes on sugar determination. J Biol Chem 195:19–23

    Google Scholar 

  • Sugie A, Naydenov N, Mizuno N, Ch Nakamura, Sh Takumi (2006) Overexpression of wheat alternative oxidase gene Waox1a alters respiration capacity and response to reactive oxygen species under low temperature in transgenic Arabidopsis. Genes Genet Syst 81:349–354

    Article  PubMed  CAS  Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol Plantarum 126:45–51

    Article  CAS  Google Scholar 

  • Thomas T, Cavicchioli R (2000) Effect of temperature on stability and activity of elongation factor 2 proteins from Antarctic and thermophilic methanogens. J Bacteriol 182:1328–1332

    Article  PubMed  CAS  Google Scholar 

  • Vandecamen A, Francoise JM, Torres BB, Maia JC, Hers HG (1989) Fructose 2, 6-bisphposphate and carbohydrate metabolism during life cycle of the aquatic fungus Balstoclafiella emersonii. J Gen Microbiol 136:137–146

    Google Scholar 

  • Vishniac HS (1996) Biodiversity of yeasts and filamentous microfungi in terrestrial Antarctic ecosystems. Biodivers Conserv 5:1365–1378

    Article  Google Scholar 

  • Voit EO (2003) Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis. J Theor Biol 223:55–78

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Ohta A, Horiuchi H, Takagi M, Imai R (2001) Multiple mechanisms regulate expression of low tempetarture-responsive (LOT) genes in Saccharomyces cerevisiae. Biochem Biophys Res Commun 283:531–535

    Article  PubMed  CAS  Google Scholar 

  • Zhang L, Onda K, Imai R, Fukuda R, Horiuchi H, Ohta A (2003) Growth temperature downshift induces antioxidant response in Saccharomyces cerevisiae. Biochem Biophys Res Commun 307:308–314

    Article  PubMed  CAS  Google Scholar 

  • Zubini P, Bertolini P, Baraldi E (2005) Variation of antioxidant enzyme gene expression during cold storage of aubergine. Acta Hort (ISHS) 682:1287–1292

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the NCSI of the Ministry of Education and Science, Bulgaria (grant VU-B-205/06) to which we owe our sincere thanks.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria B. Angelova.

Additional information

Communicated by T. Matsunaga.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gocheva, Y.G., Tosi, S., Krumova, E.T. et al. Temperature downshift induces antioxidant response in fungi isolated from Antarctica. Extremophiles 13, 273–281 (2009). https://doi.org/10.1007/s00792-008-0215-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-008-0215-1

Keywords

Navigation