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Overlapping responses between salt and oxidative stress in Debaryomyces hansenii

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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.

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References

  • 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):457–470

    CAS  PubMed  Google Scholar 

  • 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 636:656–669

    CAS  PubMed  Google Scholar 

  • 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):191–197

    CAS  PubMed  Google Scholar 

  • 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):48–60

    CAS  PubMed  Google Scholar 

  • Arino J, Ramos J, Sychrova H (2019) Monovalent cation transporters at the plasma membrane in yeasts. Yeast 36:177–193

    CAS  PubMed  Google Scholar 

  • Auesukaree C (2017) Molecular mechanisms of the yeast adaptive response and tolerance to stresses encountered during ethanol fermentation. J Biosci Bioeng 124(2):133–142

    CAS  PubMed  Google Scholar 

  • Breuer U, Harms H (2006) Debaryomyces hansenii–an extremophilic yeast with biotechnological potential. Yeast 23(6):415–437

    CAS  PubMed  Google Scholar 

  • 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):741–750

    CAS  PubMed  Google Scholar 

  • 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):11–19

    CAS  Google Scholar 

  • 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 1:73–84

    Google Scholar 

  • 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):1300–1306

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):905–911

    CAS  PubMed  Google Scholar 

  • 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):751–761

    CAS  PubMed  Google Scholar 

  • 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):1018–1024

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 606:1–9

    CAS  PubMed  Google Scholar 

  • 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):692–701

    CAS  PubMed  Google Scholar 

  • Davies MJ (2005) The oxidative environment and protein damage. Biochim Biophys Acta 1703(2):93–109

    CAS  PubMed  Google Scholar 

  • 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):2228–2240

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dormer UH, Westwater J, Stephen DW, Jamieson DJ (2002) Oxidant regulation of the Saccharomyces cerevisiae GSH1 gene. Biochim Biophysica Acta 1576(1–2):23–29

    CAS  Google Scholar 

  • Encinas JP, Lopez-Diaz TM, Garcia-Lopez ML, Otero A, Moreno B (2000) Yeast populations on Spanish fermented sausages. Meat Sci 54(3):203–208

    CAS  PubMed  Google Scholar 

  • Eruslanov E, Kusmartsev S (2010) Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 594:57–72

    CAS  PubMed  Google Scholar 

  • Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24(4):469–486

    CAS  PubMed  Google Scholar 

  • 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):e0169621

    PubMed  PubMed Central  Google Scholar 

  • 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):535–569

    CAS  PubMed  Google Scholar 

  • 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):fov099

    PubMed  PubMed Central  Google Scholar 

  • 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 100:52–60

    CAS  PubMed  Google Scholar 

  • Herrero E, Ros J, Belli G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780(11):1217–1235

    CAS  PubMed  Google Scholar 

  • Hohmann S, Mager WH (2003) Yeast Stress Responses, vol 1. Springer, Berlin

    Google Scholar 

  • 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):2307–2325

    CAS  PubMed  Google Scholar 

  • Kingsbury TJ, Cunningham KW (2000) A conserved family of calcineurin regulators. Genes Dev 14(13):1595–1604

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuang Z, Ji H, Boeke JD (2018) Stress response factors drive regrowth of quiescent cells. Curr Genet 64(4):807–810

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liang W, Ma X, Wan P, Liu L (2018) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495(1):286–291

    CAS  PubMed  Google Scholar 

  • Ma D, Li R (2013) Current understanding of HOG-MAPK pathway in Aspergillus fumigatus. Mycopathologia 175(1–2):13–23

    CAS  PubMed  Google Scholar 

  • 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):1002–1012

    CAS  PubMed  Google Scholar 

  • 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):177–184

    CAS  PubMed  Google Scholar 

  • Melamed D, Pnueli L, Arava Y (2008) Yeast translational response to high salinity: global analysis reveals regulation at multiple levels. RNA 14(7):1337–1351

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):180–188

    CAS  PubMed  Google Scholar 

  • 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):7301–7312

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):102–109

    CAS  PubMed  Google Scholar 

  • Morano KA, Grant CM, Moye-Rowley WS (2012) The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 190(4):1157–1195

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):361–366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Navarrete C, Siles A, Martinez JL, Calero F, Ramos J (2009) Oxidative stress sensitivity in Debaryomyces hansenii. FEMS Yeast Res 9(4):582–590

    CAS  PubMed  Google Scholar 

  • 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):12616–12621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Norkrans B (1966) Studies on marine occurring yeasts: growth related to pH, NaCl concentration and temperature. Archiv Mikrobiol 54:374–392

    Google Scholar 

  • Norkrans B (1968) Studies on marine occurring yeasts: respiration, fermentation and salt tolerance. Archiv Mikrobiol 62(4):358–372

    Google Scholar 

  • 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):836–845

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev 113(7):4633–4679

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):847–853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petrovic U (2006) Role of oxidative stress in the extremely salt-tolerant yeast Hortaea werneckii. FEMS Yeast Res 6(5):816–822

    CAS  PubMed  Google Scholar 

  • 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):17249–17255

    CAS  PubMed  Google Scholar 

  • 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):4005–4009

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prista C, Michan C, Miranda IM, Ramos J (2016) The halotolerant Debaryomyces hansenii, the Cinderella of non-conventional yeasts. Yeast 33(10):523–533

    CAS  PubMed  Google Scholar 

  • Ramos J, Haro R, Rodriguez-Navarro A (1990) Regulation of potassium fluxes in Saccharomyces cerevisiae. Biochim Biophys Acta 1029(2):211–217

    CAS  PubMed  Google Scholar 

  • 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):1576–1585

    CAS  PubMed  Google Scholar 

  • Reedy JL, Filler SG, Heitman J (2010) Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet Biol 47(2):107–116

    CAS  PubMed  Google Scholar 

  • 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):81–90

    CAS  PubMed  Google Scholar 

  • Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192(2):289–318

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):933–943

    CAS  PubMed  Google Scholar 

  • Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed Engl 25:1058–1071

    Google Scholar 

  • Taymaz-Nikerel H, Cankorur-Cetinkaya A, Kirdar B (2016) Genome-wide transcriptional response of Saccharomyces cerevisiae to stress-induced perturbations. Front Bioeng Biotechnol 4:17

    PubMed  PubMed Central  Google Scholar 

  • Toledano MB, Delaunay A, Monceau L, Tacnet F (2004) Microbial H2O2 sensors as archetypical redox signaling modules. Trends Biochem Sci 29(7):351–357

    CAS  PubMed  Google Scholar 

  • 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):3586–3592

    CAS  PubMed  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(2):308–314

    CAS  PubMed  Google Scholar 

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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.

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Correspondence to Carmen Michán.

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Ramos-Moreno, L., Ramos, J. & Michán, C. Overlapping responses between salt and oxidative stress in Debaryomyces hansenii. World J Microbiol Biotechnol 35, 170 (2019). https://doi.org/10.1007/s11274-019-2753-3

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