Advertisement

Overlapping responses between salt and oxidative stress in Debaryomyces hansenii

  • Laura Ramos-Moreno
  • José Ramos
  • Carmen MichánEmail author
Original Paper

Abstract

Debaryomyces hansenii is a halotolerant yeast of importance in basic and applied research. Previous reports hinted about possible links between saline and oxidative stress responses in this yeast. The aim of this work was to study that hypothesis at different molecular levels, investigating after oxidative and saline stress: (i) transcription of seven genes related to oxidative and/or saline responses, (ii) activity of two main anti-oxidative enzymes, (iii) existence of common metabolic intermediates, and (iv) generation of damages to biomolecules as lipids and proteins. Our results showed how expression of genes related to oxidative stress was induced by exposure to NaCl and KCl, and, vice versa, transcription of some genes related to osmotic/salt stress responses was regulated by H2O2. Moreover, and contrary to S. cerevisiae, in D. hansenii HOG1 and MSN2 genes were modulated by stress at their transcriptional level. At the enzymatic level, saline stress also induced antioxidative enzymatic defenses as catalase and glutathione reductase. Furthermore, we demonstrated that both stresses are connected by the generation of intracellular ROS, and that hydrogen peroxide can affect the accumulation of in-cell sodium. On the other hand, no significant alterations in lipid oxidation or total glutathione content were observed upon exposure to both stresses tested. The results described in this work could help to understand the responses to both stressors, and to improve the biotechnological potential of D. hansenni.

Keywords

Debaryomyces hansenii Gene expression Oxidative defenses ROS content Stress response 

Notes

Acknowledgements

This work was supported by XX and XXII Plan Propio Investigación, University of Córdoba to JR. We would like to thank Pemra Bakirhan for her technical assistance.

Supplementary material

11274_2019_2753_MOESM1_ESM.pdf (2.1 mb)
Supplementary material 1 (PDF 2191 kb)

References

  1. Aggarwal M, Bansal PK, Mondal AK (2005) Molecular cloning and biochemical characterization of a 3′(2′),5′-bisphosphate nucleotidase from Debaryomyces hansenii. Yeast 22(6):457–470PubMedGoogle Scholar
  2. Alhama J, Fuentes-Almagro CA, Abril N, Michan C (2018) Alterations in oxidative responses and post-translational modification caused by p, p-DDE in Mus spretus testes reveal Cys oxidation status in proteins related to cell-redox homeostasis and male fertility. Sci Total Environ 636:656–669PubMedGoogle Scholar
  3. Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J, Loureiro-Dias MC (2000) Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int J Food Microbiol 56(2–3):191–197PubMedGoogle Scholar
  4. Anderson MJ, Barker SL, Boone C, Measday V (2012) Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library. FEMS Yeast Res 12(1):48–60PubMedGoogle Scholar
  5. Arino J, Ramos J, Sychrova H (2019) Monovalent cation transporters at the plasma membrane in yeasts. Yeast 36:177–193PubMedGoogle Scholar
  6. Auesukaree C (2017) Molecular mechanisms of the yeast adaptive response and tolerance to stresses encountered during ethanol fermentation. J Biosci Bioeng 124(2):133–142PubMedGoogle Scholar
  7. Breuer U, Harms H (2006) Debaryomyces hansenii–an extremophilic yeast with biotechnological potential. Yeast 23(6):415–437PubMedGoogle Scholar
  8. Brombacher K, Fischer BB, Rufenacht K, Eggen RI (2006) The role of Yap1p and Skn7p-mediated oxidative stress response in the defence of Saccharomyces cerevisiae against singlet oxygen. Yeast 23(10):741–750PubMedGoogle Scholar
  9. Cabrera-Orefice A, Guerrero-Castillo S, Luevano-Martinez LA, Pena A, Uribe-Carvajal S (2010) Mitochondria from the salt-tolerant yeast Debaryomyces hansenii (halophilic organelles?). J Bioenergy Biomembr 42(1):11–19Google Scholar
  10. Cabrera-Orefice A, Chiquete-Felix N, Espinasa-Jaramillo J, Rosas-Lemus M, Guerrero-Castillo S, Pena A, Uribe-Carvajal S (2014) The branched mitochondrial respiratory chain from Debaryomyces hansenii: components and supramolecular organization. Biochim Biophys Acta 1:73–84Google Scholar
  11. Capaldi AP, Kaplan T, Liu Y, Habib N, Regev A, Friedman N, O’Shea EK (2008) Structure and function of a transcriptional network activated by the MAPK Hog1. Nat Genet 40(11):1300–1306PubMedPubMedCentralGoogle Scholar
  12. Carcia-Salcedo R, Montiel V, Calero F, Ramos J (2007) Characterization of DhKHA1, a gene coding for a putative Na(+) transporter from Debaryomyces hansenii. FEMS Yeast Res 7(6):905–911PubMedGoogle Scholar
  13. Chattopadhyay MK, Tabor CW, Tabor H (2006) Polyamine deficiency leads to accumulation of reactive oxygen species in a spe2Delta mutant of Saccharomyces cerevisiae. Yeast 23(10):751–761PubMedGoogle Scholar
  14. Chauhan N, Inglis D, Roman E, Pla J, Li D, Calera JA, Calderone R (2003) Candida albicans response regulator gene SSK1 regulates a subset of genes whose functions are associated with cell wall biosynthesis and adaptation to oxidative stress. Eukaryot Cell 2(5):1018–1024PubMedPubMedCentralGoogle Scholar
  15. Chawla S, Kundu D, Randhawa A, Mondal AK (2017) The serine/threonine phosphatase DhSIT4 modulates cell cycle, salt tolerance and cell wall integrity in halo tolerant yeast Debaryomyces hansenii. Gene 606:1–9PubMedGoogle Scholar
  16. Cocolin L, Urso R, Rantsiou K, Cantoni C, Comi G (2006) Dynamics and characterization of yeasts during natural fermentation of Italian sausages. FEMS Yeast Res 6(5):692–701PubMedGoogle Scholar
  17. Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703(2):93–109PubMedGoogle Scholar
  18. Dolz-Edo L, Rienzo A, Poveda-Huertes D, Pascual-Ahuir A, Proft M (2013) Deciphering dynamic dose responses of natural promoters and single cis elements upon osmotic and oxidative stress in yeast. Mol Cell Biol 33(11):2228–2240PubMedPubMedCentralGoogle Scholar
  19. Dormer UH, Westwater J, Stephen DW, Jamieson DJ (2002) Oxidant regulation of the Saccharomyces cerevisiae GSH1 gene. Biochim Biophysica Acta 1576(1–2):23–29Google Scholar
  20. Encinas JP, Lopez-Diaz TM, Garcia-Lopez ML, Otero A, Moreno B (2000) Yeast populations on Spanish fermented sausages. Meat Sci 54(3):203–208PubMedGoogle Scholar
  21. Eruslanov E, Kusmartsev S (2010) Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 594:57–72PubMedGoogle Scholar
  22. Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24(4):469–486PubMedGoogle Scholar
  23. Garcia-Neto W, Cabrera-Orefice A, Uribe-Carvajal S, Kowaltowski AJ, Alberto Luevano-Martinez L (2017) High osmolarity environments activate the mitochondrial alternative oxidase in Debaryomyces hansenii. PLoS ONE 12(1):e0169621PubMedPubMedCentralGoogle Scholar
  24. Gibson BR, Lawrence SJ, Leclaire JP, Powell CD, Smart KA (2007) Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol Rev 31(5):535–569PubMedGoogle Scholar
  25. Guma-Cintron Y, Bandyopadhyay A, Rosado W, Shu-Hu W, Nadathur GS (2015) Transcriptomic analysis of cobalt stress in the marine yeast Debaryomyces hansenii. FEMS Yeast Res 15(8):fov099PubMedPubMedCentralGoogle Scholar
  26. Herrera R, Salazar A, Ramos-Moreno L, Ruiz-Roldan C, Ramos J (2017) Vacuolar control of subcellular cation distribution is a key parameter in the adaptation of Debaryomyces hansenii to high salt concentrations. Fungal Genet Biol 100:52–60PubMedGoogle Scholar
  27. Herrero E, Ros J, Belli G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780(11):1217–1235PubMedGoogle Scholar
  28. Hohmann S, Mager WH (2003) Yeast Stress Responses, vol 1. Springer, BerlinGoogle Scholar
  29. Kavitha S, Chandra TS (2014) Oxidative stress protection and glutathione metabolism in response to hydrogen peroxide and menadione in riboflavinogenic fungus Ashbya gossypii. Appl Biochem Biotechnol 174(6):2307–2325PubMedGoogle Scholar
  30. Kingsbury TJ, Cunningham KW (2000) A conserved family of calcineurin regulators. Genes Dev 14(13):1595–1604PubMedPubMedCentralGoogle Scholar
  31. Kuang Z, Ji H, Boeke JD (2018) Stress response factors drive regrowth of quiescent cells. Curr Genet 64(4):807–810PubMedGoogle Scholar
  32. Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495(1):286–291PubMedGoogle Scholar
  33. Ma D, Li R (2013) Current understanding of HOG-MAPK pathway in Aspergillus fumigatus. Mycopathologia 175(1–2):13–23PubMedGoogle Scholar
  34. Ma N, Li C, Dong X, Wang D, Xu Y (2015) Different effects of sodium chloride preincubation on cadmium tolerance of Pichia kudriavzevii and Saccharomyces cerevisiae. J Basic Microbiol 55(8):1002–1012PubMedGoogle Scholar
  35. Martinez JL, Sychrova H, Ramos J (2011) Monovalent cations regulate expression and activity of the Hak1 potassium transporter in Debaryomyces hansenii. Fungal Genet Biol 48(2):177–184PubMedGoogle Scholar
  36. Melamed D, Pnueli L, Arava Y (2008) Yeast translational response to high salinity: global analysis reveals regulation at multiple levels. RNA 14(7):1337–1351PubMedPubMedCentralGoogle Scholar
  37. Michan C, Martinez JL, Alvarez MC, Turk M, Sychrova H, Ramos J (2013) Salt and oxidative stress tolerance in Debaryomyces hansenii and Debaryomyces fabryi. FEMS Yeast Res 13(2):180–188PubMedGoogle Scholar
  38. Minhas A, Sharma A, Kaur H, Rawal Y, Ganesan K, Mondal AK (2012) Conserved Ser/Arg-rich motif in PPZ orthologs from fungi is important for its role in cation tolerance. J Biol Chem 287(10):7301–7312PubMedPubMedCentralGoogle Scholar
  39. Montiel V, Ramos J (2007) Intracellular Na and K distribution in Debaryomyces hansenii. Cloning and expression in Saccharomyces cerevisiae of DhNHX1. FEMS Yeast Res 7(1):102–109PubMedGoogle Scholar
  40. Morano KA, Grant CM, Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190(4):1157–1195PubMedPubMedCentralGoogle Scholar
  41. Murphy MP, Holmgren A, Larsson NG, Halliwell B, Chang CJ, Kalyanaraman B, Rhee SG, Thornalley PJ, Partridge L, Gems D, Nystrom T, Belousov V, Schumacker PT, Winterbourn CC (2011) Unraveling the biological roles of reactive oxygen species. Cell Metab 13(4):361–366PubMedPubMedCentralGoogle Scholar
  42. Navarrete C, Siles A, Martinez JL, Calero F, Ramos J (2009) Oxidative stress sensitivity in Debaryomyces hansenii. FEMS Yeast Res 9(4):582–590PubMedGoogle Scholar
  43. Nomura M, Takagi H (2004) Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate. Proc Natl Acad Sci USA 101(34):12616–12621PubMedGoogle Scholar
  44. Norkrans B (1966) Studies on marine occurring yeasts: growth related to pH, NaCl concentration and temperature. Archiv Mikrobiol 54:374–392Google Scholar
  45. Norkrans B (1968) Studies on marine occurring yeasts: respiration, fermentation and salt tolerance. Archiv Mikrobiol 62(4):358–372Google Scholar
  46. Norkrans B, Kylin A (1969) Regulation of the potassium to sodium ratio and of the osmotic potential in relation to salt tolerance in yeasts. J Bacteriol 100(2):836–845PubMedPubMedCentralGoogle Scholar
  47. Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev 113(7):4633–4679PubMedPubMedCentralGoogle Scholar
  48. Paumi CM, Pickin KA, Jarrar R, Herren CK, Cowley ST (2012) Ycf1p attenuates basal level oxidative stress response in Saccharomyces cerevisiae. FEBS Lett 586(6):847–853PubMedPubMedCentralGoogle Scholar
  49. Petrovic U (2006) Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Res 6(5):816–822PubMedGoogle Scholar
  50. Posas F, Chambers JR, Heyman JA, Hoeffler JP, de Nadal E, Arino J (2000) The transcriptional response of yeast to saline stress. J Biol Chem 275(23):17249–17255PubMedGoogle Scholar
  51. Prista C, Almagro A, Loureiro-Dias MC, Ramos J (1997) Physiological basis for the high salt tolerance of Debaryomyces hansenii. Appl Environ Microbiol 63(10):4005–4009PubMedPubMedCentralGoogle Scholar
  52. Prista C, Michan C, Miranda IM, Ramos J (2016) The halotolerant Debaryomyces hansenii, the Cinderella of non-conventional yeasts. Yeast 33(10):523–533PubMedGoogle Scholar
  53. Ramos J, Haro R, Rodriguez-Navarro A (1990) Regulation of potassium fluxes in Saccharomyces cerevisiae. Biochim Biophys Acta 1029(2):211–217PubMedGoogle Scholar
  54. Ramos J, Melero Y, Ramos-Moreno L, Michan C, Cabezas L (2017) Debaryomyces hansenii strains from Valle de los Pedroches Iberian dry meat products: isolation, identification, characterization, and selection for starter cultures. J Microbiol Biotechnol 27(9):1576–1585PubMedGoogle Scholar
  55. Reedy JL, Filler SG, Heitman J (2010) Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet Biol 47(2):107–116PubMedGoogle Scholar
  56. Saijo T, Miyazaki T, Izumikawa K, Mihara T, Takazono T, Kosai K, Imamura Y, Seki M, Kakeya H, Yamamoto Y, Yanagihara K, Kohno S (2010) Skn7p is involved in oxidative stress response and virulence of Candida glabrata. Mycopathologia 169(2):81–90PubMedGoogle Scholar
  57. Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192(2):289–318PubMedPubMedCentralGoogle Scholar
  58. Segal-Kischinevzky C, Rodarte-Murguia B, Valdes-Lopez V, Mendoza-Hernandez G, Gonzalez A, Alba-Lois L (2011) The euryhaline yeast Debaryomyces hansenii has two catalase genes encoding enzymes with differential activity profile. Curr Microbiol 62(3):933–943PubMedGoogle Scholar
  59. Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058–1071Google Scholar
  60. Taymaz-Nikerel H, Cankorur-Cetinkaya A, Kirdar B (2016) Genome-wide transcriptional response of Saccharomyces cerevisiae to stress-induced perturbations. Front Bioeng Biotechnol 4:17PubMedPubMedCentralGoogle Scholar
  61. Toledano MB, Delaunay A, Monceau L, Tacnet F (2004) Microbial H2O2 sensors as archetypical redox signaling modules. Trends Biochem Sci 29(7):351–357PubMedGoogle Scholar
  62. Turk M, Montiel V, Zigon D, Plemenitas A, Ramos J (2007) Plasma membrane composition of Debaryomyces hansenii adapts to changes in pH and external salinity. Microbiology 153(Pt 10):3586–3592PubMedGoogle Scholar
  63. 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(2):308–314PubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Departamento de MicrobiologíaUniversidad de CórdobaCórdoba, EspañaSpain
  2. 2.Departamento de Bioquímica y Biología MolecularUniversidad de CórdobaCórdoba, EspañaSpain

Personalised recommendations