Table of Contents
Journal of Mycology
Volume 2014 (2014), Article ID 178274, 9 pages
http://dx.doi.org/10.1155/2014/178274
Research Article

Investigating Acid Stress Response in Different Saccharomyces Strains

1Núcleo de Pesquisas em Ciências Biológicas, Escola de Farmácia, Universidade Federal de Ouro Preto, Campus Morro do Cruzeiro, 35400-000 Ouro Preto, MG, Brazil
2Departamento de Microbiologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Campus Universitário, 30171-970 Belo Horizonte, MG, Brazil
3LBCM, Instituto de Ciências Exatas e Biológicas, Campus Morro do Cruzeiro, 35400-000 Ouro Preto, MG, Brazil

Received 3 February 2014; Accepted 1 April 2014; Published 17 April 2014

Academic Editor: Praveen Rao Juvvadi

Copyright © 2014 Rogelio Lopes Brandão et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. Trabalzini, A. Paffetti, A. Scaloni et al., “Proteomic response to physiological fermentation stresses in a wild-type wine strain of Saccharomyces cerevisiae,” Biochemical Journal, vol. 370, no. 1, pp. 35–46, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Platara, A. Ruiz, R. Serrano, A. Palomino, F. Moreno, and J. Ariño, “The transcriptional response of the yeast Na+-ATPase ENA1 gene to alkaline stress involves three main signaling pathways,” The Journal of Biological Chemistry, vol. 281, no. 48, pp. 36632–36642, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. Y. Araki, H. Wu, H. Kitagaki, T. Akao, H. Takagi, and H. Shimoi, “Ethanol stress stimulates the Ca2+-mediated calcineurin/Crz1 pathway in Saccharomyces cerevisiae,” Journal of Bioscience and Bioengineering, vol. 107, no. 1, pp. 1–6, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Daquinag, M. Fadri, S. Y. Jung, J. Qin, and J. Kunz, “The yeast PH domain proteins Slm1 and Slm2 are targets of sphingolipid signaling during the response to heat stress,” Molecular and Cellular Biology, vol. 27, no. 2, pp. 633–650, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Ariño, “Integrative responses to high pH stress in S. cerevisiae,” OMICS A Journal of Integrative Biology, vol. 14, no. 5, pp. 517–523, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. A. P. Gasch, P. T. Spellman, C. M. Kao et al., “Genomic expression programs in the response of yeast cells to environmental changes,” Molecular Biology of the Cell, vol. 11, no. 12, pp. 4241–4257, 2000. View at Google Scholar · View at Scopus
  7. H. F. De Melo, B. M. Bonini, J. Thevelein, D. A. Simões, and M. A. Morais Jr., “Physiological and molecular analysis of the stress response of Saccharomyces cerevisiae imposed by strong inorganic acid with implication to industrial fermentations,” Journal of Applied Microbiology, vol. 109, no. 1, pp. 116–127, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. A. K.-L. Chen, C. Gelling, P. L. Rogers, I. W. Dawes, and B. Rosche, “Response of Saccharomyces cerevisiae to stress-free acidification,” Journal of Microbiology, vol. 47, no. 1, pp. 1–8, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. H. C. Causton, B. Ren, S. S. K. Sang Seok Koh et al., “Remodeling of yeast genome expression in response to environmental changes,” Molecular Biology of the Cell, vol. 12, no. 2, pp. 323–337, 2001. View at Google Scholar · View at Scopus
  10. R. Serrano, A. Ruiz, D. Bernal, J. R. Chambers, and J. Ariño, “The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling,” Molecular Microbiology, vol. 46, no. 5, pp. 1319–1333, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. R. Serrano, H. Martín, A. Casamayor, and J. Ariño, “Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway,” The Journal of Biological Chemistry, vol. 281, no. 52, pp. 39785–39795, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Viladevall, R. Serrano, A. Ruiz et al., “Characterization of the calcium-mediated response to alkaline stress in Saccharomyces cerevisiae,” The Journal of Biological Chemistry, vol. 279, no. 42, pp. 43614–43624, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Karababa, E. Valentino, G. Pardini, A. T. Coste, J. Bille, and D. Sanglard, “CRZ1, a target of the calcineurin pathway in Candida albicans,” Molecular Microbiology, vol. 59, no. 5, pp. 1429–1451, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Wang, Y. Liang, B. Zhang, W. Zheng, L. Xing, and M. Li, “Alkaline stress triggers an immediate calcium fluctuation in Candida albicans mediated by Rim101p and Crz1p transcription factors,” FEMS Yeast Research, vol. 11, no. 5, pp. 430–439, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. S. H. Denison, “pH regulation of gene expression in fungi,” Fungal Genetics and Biology, vol. 29, no. 2, pp. 61–71, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. M. A. Peñalva, J. Tilburn, E. Bignell, and H. N. Arst Jr., “Ambient pH gene regulation in fungi: making connections,” Trends in Microbiology, vol. 16, no. 6, pp. 291–300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Kawahata, K. Masaki, T. Fujii, and H. Iefuji, “Yeast genes involved in response to lactic acid and acetic acid: acidic conditions caused by the organic acids in Saccharomyces cerevisiae cultures induce expression of intracellular metal metabolism genes regulated by Aft1p,” FEMS Yeast Research, vol. 6, no. 6, pp. 924–936, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Piper, C. O. Calderon, K. Hatzixanthis, and M. Mollapour, “Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives,” Microbiology, vol. 147, no. 10, pp. 2635–2642, 2001. View at Google Scholar · View at Scopus
  19. M. G. Cabral, I. Sá-Correia, and C. A. Viegas, “Adaptative responses in yeast to the herbicide 2-methyl-4- chlorophenoxyacetic acid at the level of intracellular pH homeostasis,” Journal of Applied Microbiology, vol. 96, no. 3, pp. 603–612, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Mollapour and P. W. Piper, “Targeted gene deletion in Zygosaccharomyces bailii,” Yeast, vol. 18, no. 10, pp. 173–186, 2001. View at Google Scholar
  21. P. Eraso and C. Gancedo, “Activation of yeast plasma membrane ATPase by acid pH during growth,” FEBS Letters, vol. 224, no. 1, pp. 187–192, 1987. View at Google Scholar · View at Scopus
  22. S. Claret, X. Gatti, F. Doignon, D. Thoraval, and M. Crouzet, “The Rgd1p Rho GTPase-activating protein and the Mid2p cell wall sensor are required at low pH for protein kinase C pathway activation and cell survival in Saccharomyces cerevisiae,” Eukaryotic Cell, vol. 4, no. 8, pp. 1375–1386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. X. Gatti, G. De Bettignies, S. Claret, F. Doignon, M. Crouzet, and D. Thoraval, “RGD1, encoding a RhoGAP involved in low-pH survival, is an Msn2p/Msn4p regulated gene in Saccharomyces cerevisiae,” Gene, vol. 351, pp. 159–169, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Fernandes, O. Roumanie, S. Claret et al., “The Rho3 and Rho4 small GTPases interact functionally with Wsc1p, a cell surface sensor of the protein kinase C cell-integrity pathway in Saccharomyces cerevisiae,” Microbiology, vol. 152, no. 3, pp. 695–708, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. K. W. Cunningham, “Acidic calcium stores of Saccharomyces cerevisiae,” Cell Calcium, vol. 50, no. 2, pp. 129–138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. T. K. Matsumoto, A. J. Ellsmore, S. G. Cessna et al., “An osmotically induced cytosolic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae,” The Journal of Biological Chemistry, vol. 277, no. 36, pp. 33075–33080, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. M. Bonilla and K. W. Cunningham, “Mitogen-activated protein kinase stimulation of Ca2+ signaling is required for survival of endoplasmic reticulum stress in yeast,” Molecular Biology of the Cell, vol. 14, no. 10, pp. 4296–4305, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. C.-V. Popa, I. Dumitru, L. L. Ruta, A. F. Danet, and I. C. Farcasanu, “Exogenous oxidative stress induces Ca2+ release in the yeast Saccharomyces cerevisiae,” FEBS Journal, vol. 277, no. 19, pp. 4027–4038, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Dos Santos Sant'Ana, L. Da Silva Paes, A. F. Vieira Paiva et al., “Protective effect of ions against cell death induced by acid stress in Saccharomyces,” FEMS Yeast Research, vol. 9, no. 5, pp. 701–712, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. T. A. Krulwich, R. Agus, M. Schneier, and A. A. Guffanti, “Buffering capacity of bacilli that grow at different pH ranges,” Journal of Bacteriology, vol. 162, no. 2, pp. 768–772, 1985. View at Google Scholar · View at Scopus
  31. J. Becher Dos Passos, M. Vanhalewyn, R. Lopes Brandao, I. M. Castro, J. R. Nicoli, and J. M. Thevelein, “Glucose-induced activation of plasma membrane H+-ATPase in mutants of the yeast Saccharomyces cerevisiae affected in cAMP metabolism, cAMP-dependent protein phosphorylation and the initiation of glycolysis,” Biochimica et Biophysica Acta: Molecular Cell Research, vol. 1136, no. 1, pp. 57–67, 1992. View at Publisher · View at Google Scholar · View at Scopus
  32. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, “Protein measurement with the Folin phenol reagent,” The Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951. View at Google Scholar · View at Scopus
  33. R. Tisi, S. Baldassa, F. Belotti, and E. Martegani, “Phospholipase C is required for glucose-induced calcium influx in budding yeast,” FEBS Letters, vol. 520, no. 1–3, pp. 133–138, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. M. C. Pereira, N. M. Vieira, M. R. Tótola, and M. C. M. Kasuya, “Total fatty acid composition in the characterization and identification of orchid mycorrhizal fungi Epulorhiza spp,” Revista Brasileira de Ciencia do Solo, vol. 35, no. 4, pp. 1159–1165, 2011. View at Google Scholar · View at Scopus
  35. C. D. Cruz, Programa genes: diversidade genética [Ph.D. thesis], Universidade Federal de Viçosa, Viçosa, MG, Brazil, 2008.
  36. J. Sambrook, E. F. Fritsch, and T. Maniatis, Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA, 2nd edition, 1989.
  37. H. Ito, Y. Fukuda, K. Murata, and A. Kimura, “Transformation of intact yeast cells treated with alkali cations,” Journal of Bacteriology, vol. 153, no. 1, pp. 163–168, 1983. View at Google Scholar · View at Scopus
  38. A. Ruiz and J. Ariño, “Function and regulation of the Saccharomyces cerevisiae ENA sodium ATPase system,” Eukaryotic Cell, vol. 6, no. 12, pp. 2175–2183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. M. J. M. Trópia, A. S. Cardoso, R. Tisi et al., “Calcium signaling and sugar-induced activation of plasma membrane H+-ATPase in Saccharomyces cerevisiae cells,” Biochemical and Biophysical Research Communications, vol. 343, no. 4, pp. 1234–1243, 2006. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Zang, Q. Xie, J. B. Robertson, and C. H. Johnson, “pHlash: a new genetically encoded and ratiometric luminescence sensor of intracellular pH,” PLoS ONE, vol. 7, Article ID 43072, 2012. View at Google Scholar
  41. M. J. Carlisle, S. C. Watkinson, and G. W. Gooday, The Fungi, Academic Press, San Diego, Calif, USA, 2nd edition, 2001.
  42. R. Serrano, M. C. Kielland-Brandt, and G. R. Fink, “Yeast plasma membrane ATPase is essential for growth and has homology with (Na+,K+), K+ and Ca2+-ATPases,” Nature, vol. 319, no. 6055, pp. 689–693, 1986. View at Google Scholar · View at Scopus
  43. F. Portillo, “Regulation of plasma membrane H+-ATPase in fungi and plants,” Biochimica et Biophysica Acta: Reviews on Biomembranes, vol. 1469, no. 1, pp. 31–42, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. V. Carmelo, H. Santos, and I. Sá-Correia, “Effect of extracellular acidification on the activity of plasma membrane ATPase and on the cytosolic and vacuolar pH of Saccharomyces cerevisiae,” Biochimica et Biophysica Acta: Biomembranes, vol. 1325, no. 1, pp. 63–70, 1997. View at Publisher · View at Google Scholar · View at Scopus
  45. G. A. Martínez-Muñoz and P. Kane, “Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast,” The Journal of Biological Chemistry, vol. 283, no. 29, pp. 20309–20319, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Ding, X. Huang, L. Zhang, N. Zhao, D. Yang, and K. Zhang, “Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae,” Applied Microbiology and Biotechnology, vol. 85, no. 2, pp. 253–263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. N. P. Mira, M. Palma, J. F. Guerreiro, and I. Sá-Correia, “Genome-wide identification of Saccharomyces cerevisiae genes required for tolerance to acetic acid,” Microbial Cell Factories, vol. 9, article 79, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Bollo, S. Bonansea, and E. E. Machado, “Involvement of Na+/H+ exchanger in the calcium signaling in epimastigotes of Trypanosoma cruzi,” FEBS Letters, vol. 580, no. 11, pp. 2686–2690, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. J. C. Kapteyn, B. Ter Riet, E. Vink et al., “Low external ph induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall,” Molecular Microbiology, vol. 39, no. 2, pp. 469–479, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. R. M. de Lucena, C. Elsztein, D. A. Simões, and M. A. Morais Jr, “Participation of CW1, HOG and calcineurin pathways in the tolerance of Saccharomyces to low pH by inorganic acid,” Journal of Applied Microbiology, vol. 113, no. 3, pp. 629–640, 2012. View at Google Scholar