1887

Abstract

IFO1125 was found to acquire increased aluminium (Al) resistance from 50 μM to more than 5 mM by repetitive culturing with stepwise increases in Al concentration at pH 4.0. To investigate the mechanism underlying this novel phenomenon, wild-type and Al-resistant cells were compared. Neither cell type accumulated the free form of Al (Al) added to the medium. Transmission electron microscopic analyses revealed a greater number of mitochondria in resistant cells. The formation of small mitochondria with simplified cristae structures was observed in the wild-type strain grown in the presence of Al and in resistant cells grown in the absence of Al. Addition of Al to cells resulted in high mitochondrial membrane potential and concomitant generation of reactive oxygen species (ROS). Exposure to Al also resulted in elevated levels of oxidized proteins and oxidized lipids. Addition of the antioxidants -tocopherol and ascorbic acid alleviated the Al toxicity, suggesting that ROS generation is the main cause of Al toxicity. Differential display analysis indicated upregulation of mitochondrial genes in the resistant cells. Resistant cells were found to have 2.5- to 3-fold more mitochondrial DNA (mtDNA) than the wild-type strain. Analysis of tricarboxylic acid cycle and respiratory-chain enzyme activities in wild-type and resistant cells revealed significantly reduced cytochrome oxidase activity and resultant high ROS production in the latter cells. Taken together, these data suggest that the adaptive increased resistance to Al stress in resistant cells resulted from an increased number of mitochondria and increased mtDNA content, as a compensatory response to reduced respiratory activity caused by a deficiency in complex IV function.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/016048-0
2008-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/11/3437.html?itemId=/content/journal/micro/10.1099/mic.0.2007/016048-0&mimeType=html&fmt=ahah

References

  1. Aydin S., Yargicoglu P., Derin N., Aliciguzel Y., Abidin I., Agar A. 2005; The effect of chronic restraint stress and sulfite on visual evoked potentials (VEPs): relation to lipid peroxidation. Food Chem Toxicol 43:1093–1101
    [Google Scholar]
  2. Basu U., Southron J. L., Stephens J. L., Taylor G. J. 2004; Reverse genetic analysis of the glutathione metabolic pathway suggests a novel role of PHGPX and URE2 genes in aluminum resistance in Saccharomyces cerevisiae . Mol Genet Genomics 271:627–637
    [Google Scholar]
  3. Bonner W. D. 1955; Succinic dehydrogenase. Methods Enzymol 1:722–729
    [Google Scholar]
  4. Brownlee M. 2001; Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820
    [Google Scholar]
  5. Cook A., Sanwal B. D. 1969; Isocitrate dehydrogenase (NAD-specific) from Neurospora crassa . Methods Enzymol 13:42–48
    [Google Scholar]
  6. Englard S., Siegel L. 1969; Mitochondrial l-malate dehydrogenase of beef heart. Methods Enzymol 13:99–106
    [Google Scholar]
  7. Exley C. 1999; A molecular mechanism of aluminium-induced Alzheimer's disease?. J Inorg Biochem 76:133–140
    [Google Scholar]
  8. Fang J., Beattie D. S. 2003; External alternative NADH dehydrogenase of Saccharomyces cerevisiae: a potential source of superoxide. Free Radic Biol Med 34:478–488
    [Google Scholar]
  9. Fang J., Wang Y., Beattie D. S. 2001; Isolation and characterization of complex I, rotenone-sensitive NADH : ubiquinone oxidoreductase, from the procyclic forms of Trypanosoma brucei . Eur J Biochem 268:3075–3082
    [Google Scholar]
  10. Fansler B., Lowenstein J. M. 1969; Aconitase from pig heart. Methods Enzymol 13:26–30
    [Google Scholar]
  11. Frank J., Pompella A., Biesalski H. K. 2000; Histochemical visualization of oxidant stress. Free Radic Biol Med 29:1096–1105
    [Google Scholar]
  12. Hamilton C. A., Good A. G., Taylor G. J. 2001; Vacuolar H+-ATPase, but not mitochondrial F1F10-ATPase, is required for aluminum resistance in Saccharomyces cerevisiae . FEMS Microbiol Lett 205:231–236
    [Google Scholar]
  13. Hill R. L., Bradshaw R. A. 1969; Fumarase. Methods Enzymol 13:91–99
    [Google Scholar]
  14. Hiradate S. 2004; Speciation of aluminum in soil environments. Soil Sci Plant Nutr 50:303–314
    [Google Scholar]
  15. Hiradate S., Taniguchi S., Sakurai K. 1998; Aluminum speciation in aluminum silica solutions and potassium chloride extracts of acidic soils. Soil Sci Soc Am J 62:630–636
    [Google Scholar]
  16. Illias R. M., Sinclair R., Robertson D., Neu A., Chapman S. K., Reid G. A. 1998; l-Mandelate dehydrogenase from Rhodotorula graminis: cloning, sequencing, and kinetic characterization of the recombinant enzyme and its independently expressed flavin domain. Biochem J 333:107–115
    [Google Scholar]
  17. Jezek P., Hlavata L. 2005; Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism. Int J Biochem Cell Biol 37:2478–2503
    [Google Scholar]
  18. Kagawa Y., Yoshida M. 1979; Soluble ATPase (F1) from a thermophilic bacterium: purification, dissociation into subunits, and reconstitution from individual subunits. Methods Enzymol 55:781–787
    [Google Scholar]
  19. Kakimoto M., Kobayashi A., Fukuda R., Ono Y., Ohta A., Yoshimura E. 2005; Genome-wide screening of aluminum tolerance in Saccharomyces cerevisiae . Biometals 18:467–474
    [Google Scholar]
  20. Kawahara M. 2005; Effects of aluminum on the nervous system and its possible link with neurodegenerative diseases. J Alzheimers Dis 8:171–182 discussion 209–15
    [Google Scholar]
  21. Kawai F., Zhang D., Sugimoto M. 2000; Isolation and characterization of acid- and Al-tolerant microorganisms. FEMS Microbiol Lett 189:143–147
    [Google Scholar]
  22. Kobayashi Y., Yamamoto Y., Matsumoto H. 2004; Studies on the mechanism of aluminum tolerance in pea ( Pisum sativum L.) using aluminum-tolerant cultivar ‘Alaska’ and aluminum-sensitive cultivar ‘Hyogo’. Soil Sci Plant Nutr 50:197–204
    [Google Scholar]
  23. Ma J. F., Ryan P. R., Delhaize E. 2001; Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278
    [Google Scholar]
  24. MacDiarmid C. W., Gardner R. C. 1996; Al toxicity in yeast. Plant Physiol 112:1101–1109
    [Google Scholar]
  25. MacDiarmid C. W., Gardner R. C. 1998; Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion. J Biol Chem 273:1727–1732
    [Google Scholar]
  26. Middaugh J., Hamel R., Baptiste G. J., Beriault R., Chenier D., Appanna V. D. 2005; Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase. J Biol Chem 280:3159–3165
    [Google Scholar]
  27. Nichols B. J., Rigoulet M., Denton R. M. 1994; Comparison of the effects of Ca2+, adenine nucleotides and pH on the kinetic properties of mitochondrial NAD+-isocitrate dehydrogenase and oxoglutarate dehydrogenase from the yeast Saccharomyces cerevisiae and rat heart. Biochem J 303:461–465
    [Google Scholar]
  28. Oyedotun K. S., Lemire B. D. 2001; The quinone-binding sites of the Saccharomyces cerevisiae succinate-ubiquinone oxidoreductase. J Biol Chem 276:16936–16943
    [Google Scholar]
  29. Sakai Y., Ishikawa J., Fukasaka S., Yurimoto H., Mitsui R., Yanase H., Kato N. 1999; A new carboxylesterase from Brevibacterium linens IFO12171 responsible for the conversion of 1,4-butanediol diacrylate to 4-hydroxybutyl acrylate: purification, characterization, gene cloning, and gene expression in Escherichia coli . Biosci Biotechnol Biochem 63:688–697
    [Google Scholar]
  30. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Samokhvalov V., Ignatov V., Kondrashova M. 2004; Inhibition of Krebs cycle and activation of glyoxylate cycle in the course of chronological aging of Saccharomyces cerevisiae. Compensatory role of succinate oxidation. Biochimie 86:39–46
    [Google Scholar]
  32. Sherman F. 1991; Getting started with yeast. Methods Enzymol 194:3–20
    [Google Scholar]
  33. Srere P. A. 1969; Citrate synthase. Methods Enzymol 13:3–11
    [Google Scholar]
  34. Tani A., Zhang D., Duine J. A., Kawai F. 2004; Treatment of the yeast Rhodotorula glutinis with AlCl3 leads to adaptive acquirement of heritable aluminum resistance. Appl Microbiol Biotechnol 65:344–348
    [Google Scholar]
  35. Wang Y., Fang J., Leonard S. S., Rao K. M. 2004; Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 36:1434–1443
    [Google Scholar]
  36. Yakimova E. T., Kapchina-Toteva V. M., Woltering E. J. 2007; Signal transduction events in aluminum-induced cell death in tomato suspension cells. J Plant Physiol 164:702–708
    [Google Scholar]
  37. Yamamoto Y., Kobayashi Y., Devi S. R., Rikiishi S., Matsumoto H. 2002; Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72
    [Google Scholar]
  38. Zheng K., Pan J. W., Ye L., Fu Y., Peng H. Z., Wan B. Y., Gu Q., Bian H. W., Han N. other authors 2007; Programmed cell death-involved aluminum toxicity in yeast alleviated by antiapoptotic members with decreased calcium signals. Plant Physiol 143:38–49
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/016048-0
Loading
/content/journal/micro/10.1099/mic.0.2007/016048-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error