1887

Abstract

The heat shock (HS) response is an adaptation of organisms to elevated temperature. It includes substantial changes in the composition of cellular membranes, proteins and soluble carbohydrates. To protect the cellular macromolecules, thermophilic organisms have evolved mechanisms of persistent thermotolerance. Many of those mechanisms are common for thermotolerance and the HS response. However, it remains unknown whether thermophilic species respond to HS by further elevating concentrations of protective components. We investigated the composition of the soluble cytosol carbohydrates and membrane lipids of the thermophilic fungi and at optimum temperature conditions (41–43 °С), and under HS (51–53 °С). At optimum temperatures, the membrane lipid composition was characterized by a high proportion of phosphatidic acids (PA) (20–35 % of the total), which were the main components of the membrane lipids, together with phosphatidylcholines (PC), phosphatidylethanolamines (PE) and sterols (St). In response to HS, the proportion of PA and St increased, and the amount of PC and PE decreased. No decrease in the degree of fatty acid desaturation in the major phospholipids under HS was detected. The mycelium of all fungi at optimum temperatures contained high levels of trehalose (8–10 %, w/w; 60–95 % of the total carbohydrates), which is a hallmark of thermophilia. In contrast to mesophilic fungi, heat exposure decreased the trehalose level and the fungi did not acquire thermotolerance to lethal HS, indicating that trehalose plays a key role in this process. This pattern of changes appears to be conserved in the studied filamentous thermophilic fungi.

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2016-06-01
2024-04-19
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References

  1. Balogh G., Péter M., Glatz A., Gombos I., Török Z., Horváth I., Harwood J. L., Vígh L. 2013; . Key role of lipids in heat stress management. FEBS Lett 587:1970–1980 [View Article][PubMed]
    [Google Scholar]
  2. Benning C., Huang Z. H., Gage D. A. 1995; Accumulation of a novel glycolipid and a betaine lipid in cells of Rhodobacter sphaeroides grown under phosphate limitation. Arch Biochem Biophys 317:103–111 [View Article][PubMed]
    [Google Scholar]
  3. Brobst K. M. 1972; Gas–liquid chromatography of trimethylsilyl derivatives: analysis of corn syrup. In Methods of Carbohydrate Chemistry pp. 3–8 Edited by Whistler R. L., BeMiller J. N. New York, London: Academic Press;
    [Google Scholar]
  4. Crowe J. H. 2007; Trehalose as a "chemical chaperone". In Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks ( Advances in Experimental Medicine and Biology) Vol. 594 pp. 143–158 Edited by Csermely P., Vígh L. New York: Springer; [CrossRef]
    [Google Scholar]
  5. Daugaard M., Rohde M., Jäättelä M. 2007; The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Lett 581:3702–3710 [View Article][PubMed]
    [Google Scholar]
  6. De Virgilio C., Hottiger T., Dominguez J., Boller T., Wiemken A. 1994; The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. Eur J Biochem 219:179–186[PubMed] [CrossRef]
    [Google Scholar]
  7. Elbein A. D., Pan Y. T., Pastuszak I., Carroll D. 2003; New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R [View Article][PubMed]
    [Google Scholar]
  8. Garton G. A., Goodwin T. W., Lijinsky W. 1951; Studies in carotenogenesis; general conditions governing beta-carotene synthesis by the fungus Phycomyces blakesleeanus Burgeff. Biochem J 48:154–163[PubMed] [CrossRef]
    [Google Scholar]
  9. Hazel J. R. 1995; . Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?. Annu Rev Physiol 57:19–42 [View Article][PubMed]
    [Google Scholar]
  10. Iturriaga G., Suárez R., Nova-Franco B. 2009; Trehalose metabolism: from osmoprotection to signaling. Int J Mol Sci 10:3793–3810 [View Article][PubMed]
    [Google Scholar]
  11. Jepsen H. F., Jensen B. 2004; Accumulation of trehalose in the thermophilic fungus Chaetomium thermophilum var. coprophilum in response to heat or salt stress. Soil Biol Biochem 36:1669–1674 [View Article]
    [Google Scholar]
  12. Kates M. 1972; Techniques of lipidology: Isolation, analysis and identification of lipids. In Laboratory Techniques in Biochemistry and Molecular Biology Vol. 3 pp. 267–610 Edited by Work T. S., Work E. Amsterdam: North-Holland Publishing; [CrossRef]
    [Google Scholar]
  13. Kim I. S., Moon H. Y., Yun H. S., Jin I. 2006; Heat shock causes oxidative stress and induces a variety of cell rescue proteins in Saccharomyces cerevisiae KNU5377. J Microbiol 44:492–501[PubMed]
    [Google Scholar]
  14. Kooijman E. E., Chupin V., de Kruijff B., Burger K. N. 2003; Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4:162–174[PubMed] [CrossRef]
    [Google Scholar]
  15. Magan N. 2007; Fungi in extreme environments. In Environmental and Microbial Relationships, 2nd edn. Vol. 4 pp. 85–103 Edited by Kubicek C. P., Druzhinina I. S. Berlin, Heidelberg: Springer;
    [Google Scholar]
  16. Maheshwari R., Bharadwaj G., Bhat M. K. 2000; Thermophilic fungi: their physiology and enzymes. Microbiol Mol Biol Rev 64:461–488[PubMed] [CrossRef]
    [Google Scholar]
  17. McMahon H. T., Gallop J. L. 2005; Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:590–596 [View Article][PubMed]
    [Google Scholar]
  18. Meyer F., Bloch K. 1963; . Effect of temperature on the enzymatic synthesis of unsaturated fatty acids in Torulopsis utillis . Biochim Biophys Acta 77:671–673 [CrossRef]
    [Google Scholar]
  19. Mumma R. O., Fergus C. L., Sekura R. D. 1970; . The lipids of thermophilic fungi: lipid composition comparisons between thermophilic and mesophilic fungi. Lipids 5:100–103[PubMed] [CrossRef]
    [Google Scholar]
  20. Mumma R. O., Sekura R. D., Fergus C. L. 1971; . Thermophilic fungi: III. the lipids of Humicola grisea var.thermoidea . Lipids 6:589–594 [CrossRef]
    [Google Scholar]
  21. Nichols B. W. 1963; Separation of the lipids of photosynthetic tissues: improvements in analysis by thin-layer chromatography. Biochim Biophys Acta 70:417–422[PubMed] [CrossRef]
    [Google Scholar]
  22. Oberson J., Rawyler A., Brändle R., Canevascini G. 1999; Analysis of the heat-shock response displayed by two Chaetomium species originating from different thermal environments. Fungal Genet Biol 26:178–189 [View Article][PubMed]
    [Google Scholar]
  23. Panaretou B., Zhai C. 2008; . The heat shock proteins: their roles as multi-component machines for protein folding. Fungal Biol Rev 22:110–119 [CrossRef]
    [Google Scholar]
  24. Piper P. W. 1993; Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae . FEMS Microbiol Rev 11:339–355[PubMed] [CrossRef]
    [Google Scholar]
  25. Raju K. S., Maheshwari R., Sastry P. S. 1976; . Lipids of some thermophilic fungi. Lipids 11:741–746 [CrossRef]
    [Google Scholar]
  26. Reinders A., Romano I., Wiemken A., De Virgilio C. 1999; . The thermophilic yeast Hansenula polymorpha does not require trehalose synthesis for growth at high temperatures but does for normal acquisition of thermotolerance. J Bacteriol 181:4665–4668[PubMed]
    [Google Scholar]
  27. Richter K., Haslbeck M., Buchner J. 2010; The heat shock response: life on the verge of death. Mol Cell 40:253–266 [View Article][PubMed]
    [Google Scholar]
  28. Sadovova N. V., Feofilova E. P. 1989; . Properties of lipid composition in the thermophilic fungus Myceliophthora thermophila . Microbiology 58:169–174
    [Google Scholar]
  29. Sadovova N. V., Feofilova E. P., Gryaznova M. 1991a; Lipid composition of subcellular fractions and trehalose synthesis in Myceliophthora thermophila . Microbiology 59:495–500
    [Google Scholar]
  30. Sadovova N. V., Gryaznova M. V., Tereshina V. M., Feofilova E. P., Khomidov K. S., Egorova T. A. 1991b; . Peculiarities of the biochemical adaptation of the thermophilic fungus Myceliophthora thermophila to temperature stress. Appl Biochem Microbiol 26:447–453
    [Google Scholar]
  31. Sinensky M. 1974; . Homeoviscous adaptation--a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli . Proc Natl Acad Sci U S A 71:522–525[PubMed] [CrossRef]
    [Google Scholar]
  32. Singer M. A., Lindquist S. 1998; Multiple effects of trehalose on protein folding in vitro and in vivo. Mol Cell 1:639–648[PubMed] [CrossRef]
    [Google Scholar]
  33. Somogyi M. 1945; . Determination of blood sugar. J Biol Chem 160:69–73
    [Google Scholar]
  34. Tereshina V. M., Memorskay A. S., Kotlova E. R., Feofilova E. P. 2010; . Membrane lipid and cytosol carbohydrate composition in Aspergillus niger under heat shock. Microbiology 79:40–46 [CrossRef]
    [Google Scholar]
  35. Tereshina V. M., Memorskaya A. S., Kotlova E. R. 2011; . The effect of different heat influences on composition of membrane lipids and cytosol carbohydrates in mycelial fungi. Microbiology 80:455–460 [CrossRef]
    [Google Scholar]
  36. Trent J. D., Gabrielsen M., Jensen B., Neuhard J., Olsen J. 1994; . Acquired thermotolerance and heat shock proteins in thermophiles from the three phylogenetic domains. J Bacteriol 176:6148–6152[PubMed]
    [Google Scholar]
  37. Vigh L., Escribá P. V., Sonnleitner A., Sonnleitner M., Piotto S., Maresca B., Horváth I., Harwood J. L. 2005; . The significance of lipid composition for membrane activity: new concepts and ways of assessing function. Prog Lipid Res 44:303–344 [View Article][PubMed]
    [Google Scholar]
  38. Weete J. D. 1974; Introduction to fungal lipids. In Fungal Lipid Biochemistry, 1st edn. pp. 3–36 Edited by Kritchevsky D. New York: Springer; [CrossRef]
    [Google Scholar]
  39. Wharton D. A. 2002; The hot club. In Life at the Limits: Organisms in Extreme Environments pp. 129–149 Cambridge: Cambridge University Press; [CrossRef]
    [Google Scholar]
  40. Yanutsevich E. A., Memorskaya A. S., Groza N. V., Kochkina G. A., Tereshina V. M. 2014; Heat shock response in the thermophilic fungus Rhizomucor miehei . Microbiology 83:498–504 [View Article]
    [Google Scholar]
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