The yeast hypoxic responses, resources for new biotechnological opportunities

Biotechnology Letters

Volumn 34, Issue 12, 2012, Pages 2161-2173

  Siso, M Isabel González ^a   Becerra, Manuel ^a   Maceiras, Mónica Lamas ^a   Vázquez, Ángel Vizoso ^a   Cerdán, M Esperanza ^a  

^a UNIVERSITY OF A CORUÑA   (Spain)

Author keywords

Heme sensing; Hypoxia; Sterol sensing molecular; Yeast bio productions; Yeast pathogen virulence

Indexed keywords

BIOTECHNOLOGICAL APPLICATIONS; GLUTATHIONES; HEME-SENSING; HYPOXIA; LOW OXYGEN; MOLECULAR MECHANISM; STEROL SENSING; TARGET GENES;

BIOSYNTHESIS; BIOTECHNOLOGY; ETHANOL; MOLECULAR OXYGEN; PORPHYRINS; RECOMBINANT PROTEINS;

YEAST;

ALCOHOL; GLUTATHIONE; OXYGEN; RECOMBINANT PROTEIN; VIRULENCE FACTOR;

ANAEROBIC GROWTH; BIOTECHNOLOGY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; REVIEW; YEAST;

ANAEROBIOSIS; BIOTECHNOLOGY; ETHANOL; GENE EXPRESSION REGULATION, FUNGAL; GLUTATHIONE; OXYGEN; RECOMBINANT PROTEINS; STRESS, PHYSIOLOGICAL; VIRULENCE FACTORS; YEASTS;

EID: 84868453711     PISSN: 01415492     EISSN: 15736776     Source Type: Journal    
DOI: 10.1007/s10529-012-1039-8     Document Type: Review

References (71)

1. Abramova NE, Cohen BD, Sertil O, Kapoor R, Davies KJ, Lowry CV (2001) Regulatory mechanisms controlling expression of the DAN/TIR mannoprotein genes during anaerobic remodeling of the cell wall in Saccharomyces cerevisiae. Genetics 157: 1169-1177.
2. Askew C, Sellam A, Epp E, Hogues H, Mullick A, Nantel A, Whiteway M (2009) Transcriptional regulation of carbohydrate metabolism in the human pathogen Candida albicans. PLoS Pathog 5: e1000612.
3. Aslett M, Wood V (2006) Gene Ontology annotation status of the fission yeast genome: preliminary coverage approaches 100%. Yeast 23: 913-919.
4. Bao WG, Guiard B, Fang ZA, Donnini C, Gervais M, Passos FM, Ferrero I, Fukuhara H, Bolotin-Fukuhara M (2008) Oxygen-dependent transcriptional regulator Hap1p limits glucose uptake by repressing the expression of the major glucose transporter gene RAG1 in Kluyveromyces lactis. Eukaryot Cell 11: 1895-1905.
5. Barker BM, Kroll K, Vödisch M, Mazurie A, Kniemeyer O, Cramer RA (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13: e62.
6. Baumann K, Maurer M, Dragosits M, Cos O, Ferrer P, Mattanovich D (2008) Hypoxic fed-batch cultivation of Pichia pastoris increases specific and volumetric productivity of recombinant proteins. Biotechnol Bioeng 100: 177-183.
7. Baumann K, Carnicer M, Dragosits M, Graf AB, Stadlmann J, Jouhten P, Maaheimo H, Gasser B, Albiol J, Mattanovich D, Ferrer P (2010) A multi-level study of recombinant Pichia pastoris in different oxygen conditions. BMC Syst Biol 4: e141.
8. Baumann K, Dato L, Graf AB, Frascotti G, Dragosits M, Porro D, Mattanovich D, Ferrer P, Branduardi P (2011) The impact of oxygen on the transcriptome of recombinant S. cerevisiae and P. pastoris, a comparative analysis. BMC Genomics 12: e218.
9. Becerra M, Lombardía-Ferreira LJ, Hauser NC, Hoheisel JD, Tizon B, Cerdán ME (2002) The yeast transcriptome in aerobic and hypoxic conditions: effects of hap1, rox1, rox3 and srb10 deletions. Mol Microbiol 43: 545-555.
10. Bien CM, Espenshade PJ (2010) Sterol regulatory element binding proteins in fungi: hypoxic transcription factors linked to pathogenesis. Eukaryot Cell 9: 352-359.
11. Castro Prego R, Lamas Maceiras M, Soengas P, Carneiro I, González Siso MI, Cerdán ME (2010a) Regulatory factors controlling transcription of Saccharomyces cerevisiaeIXR1 (ORD1) by oxygen levels. A model of transcriptional adaptation from aerobiosis to hypoxia implicating ROX1 and IXR1 cross-regulation. Biochem J 425: 235-243.
12. Castro Prego R, Lamas Maceiras M, Soengas P, Fernández Leiro R, Carneiro I, Becerra M, González-Siso MI, Cerdán ME (2010b) Ixr1p regulates oxygen-dependent HEM13 transcription. FEMS Yeast Res 10: 309-321.
13. Chantrel Y, Gaisne M, Lions C, Verdière J (1998) The transcriptional regulator Hap1p (Cyp1p) is essential for anaerobic or heme-deficient growth of Saccharomyces cerevisiae: genetic and molecular characterization of an extragenic suppressor that encodes a WD repeat protein. Genetics 148: 559-569.
14. Chen Y, Yang X, Zhang S, Wang X, Guo C, Guo X, Xiao D (2012) Development of Saccharomyces cerevisiae producing higher levels of sulfur dioxide and glutathione to improve beer flavor stability. Appl Biochem Biotechnol 166: 402-413.
15. Chun CD, Liu OW, Madhani HD (2007) A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans. PLoS Pathog 3: e22.
16. Clifton IJ, McDonough MA, Ehrismann D, Kershaw NJ, Granatino N, Schofield CJ (2006) Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J Inorg Biochem 100: 644-669.
17. Cordente AG, Heinrich A, Pretorius IS, Swiegers JH (2009) Isolation of sulfite reductase variants of a commercial wine yeast with significantly reduced hydrogen sulfide production. FEMS Yeast Res 9: 446-459.
18. Davies BS, Rine J (2006) A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 174: 91-201.
19. de Groot M, Daran-Lapujade P, van Breukelen B, Knijnenburg T, de Hulster E, Reinders M, Pronk J, Heck A, Slijper M (2007) Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 153: 3864-3878.
20. Dueñas-Sánchez R, Gutiérrez G, Rincón AM, Codón AC, Benítez T (2012) Transcriptional regulation of fermentative and respiratory metabolism in Saccharomyces cerevisiae industrial bakers' strains. FEMS Yeast Res. doi: 10. 1111/j. 1567-1364. 2012. 00813. x.
21. Ernst JF, Tielker D (2009) Responses to hypoxia in fungal pathogens. Cell Microbiol 11: 183-190.
22. Farhana A, Guidry L, Srivastava A, Singh A, Hondalus MK, Steyn AJC (2010) Reductive stress in microbes: implications for understanding mycobacterium tuberculosis disease and persistence. Adv Microb Physiol 57: 43-117.
23. Frand A, Kaiser C (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1: 161-170.
24. Gasser B, Sauer M, Maurer M, Stadlmayr G, Mattanovich D (2007) Transcriptomics-based identification of novel factors enhancing heterologous protein secretion in yeasts. Appl Environ Microbiol 73: 6499-6507.
25. Gómez-Pastor R, Pérez-Torrado R, Matallana E (2012) Modification of the TRX2 gene dose in Saccharomyces cerevisiae affects hexokinase 2 gene regulation during wine yeast biomass production. Appl Microbiol Biotechnol 94: 773-787.
26. González Siso MI, Freire Picos MA, Cerdán ME (1996) Reoxidation of the NADP produced by the pentose phosphate pathway is necessary for the utilization of glucose by Kluyveromyces lactis rag2 mutants. FEBS Lett 387: 7-10.
27. Guida A, Lindstädt C, Maguire SL, Ding C, Higgins DG, Corton NJ, Berriman M, Butler G (2011) Using RNA-seq to determine the transcriptional landscape and the hypoxic response of the pathogenic yeast Candida parapsilosis. BMC Genomics 12: e628.
28. Hara KY, Kiriyama K, Inagaki A, Nakayama H, Kondo A (2012) Improvement of glutathione production by metabolic engineering the sulfate assimilation pathway of Saccharomyces cerevisiae. Appl Microbiol Biotechnol 94: 1313-1319.
29. Henri J, Rispal D, Bayart E, van Tilbeurgh H, Séraphin B, Graille M (2010) Structural and functional insights into Saccharomyces cerevisiae Tpa1, a putative prolylhydroxylase influencing translation termination and transcription. J Biol Chem 285: 30767-30778.
30. Hickman MJ, Spatt D, Winston F (2011) The Hog1 mitogen-activated protein kinase mediates a hypoxic response in Saccharomyces cerevisiae. Genetics 188: 325-338.
31. Hon T, Lee HC, Hach A, Johnson JL, Craig EA, Erdjument-Bromage H, Tempst P, Zhang L (2001) The Hsp70-Ydj1 molecular chaperone represses the activity of the heme activator protein Hap1 in the absence of heme. Moll Cell Biol 21: 7923-7932.
32. Hughes BT, Espenshade PJ (2008) Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl-hydroxylase family member. EMBO J 27: 1491-1501.
33. Hughes AL, Todd BL, Espenshade PJ (2005) SREBP pathway responds to sterols and functions as an oxygen sensor in fission yeast. Cell 120: 831-842.
34. Jiang Y, Vasconcelles MJ, Wretzel S, Light A, Martin CE, Goldberg MA (2001) MGA2 is involved in the low-oxygen response element-dependent hypoxic induction of genes in Saccharomyces cerevisiae. Mol Cell Biol 21: 6161-6169.
35. Kandasamy P, Vemula M, Oh CS, Chellappa R, Martin CE (2004) Regulation of unsaturated fatty acid biosynthesis in Saccharomyces: the endoplasmic reticulum membrane protein, Mga2p, a transcription activator of the OLE1 gene, regulates the stability of the OLE1 mRNA through exosome-mediated mechanisms. J Biol Chem 279: 36586-36592.
36. Keng T (1992) HAP1 and ROX1 form a regulatory pathway in the repression of HEM13 transcription in Saccharomyces cerevisiae. Mol Cell Biol 12: 2616-2623.
37. Klinkenberg LG, Mennella TA, Luetkenhaus K, Zitomer RS (2005) Combinatorial repression of the hypoxic genes of Saccharomyces cerevisiae by DNA binding proteins Rox1 and Mot3. Eukaryot Cell 4: 649-660.
38. Lamas Maceiras M, Núñez L, Rodríguez Belmonte E, González Siso MI, Cerdán ME (2007) Functional characterization of KlHAP1: a model to foresee different mechanisms of transcriptional regulation by Hap1p in yeasts. Gene 405: 96-107.
39. Lamas Maceiras M, Freire-Picos MA, Rodríguez Torres AM (2010) Transcriptional repression by Kluyveromyces lactis Tup1 in Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 38: 79-84.
40. Lamas Maceiras M, Rodríguez Torres MA, Freire Picos MA (2011) A stress response related to the carbon source and the absence of KlHAP2 in Kluyveromyces lactis. J Ind Microbiol Biotechnol 38: 43-49.
41. Lando D, Balmer J, Laue ED, Kouzarides T (2012) The S. pombe histone H2A dioxygenase Ofd2 regulates gene expression during hypoxia. PLoS ONE 7: e29765.
42. Lee H, Bien CM, Hughes AL, Espenshade PJ, Kwon-Chung KJ, Chang YC (2007) Cobalt chloride, a hypoxia-mimicking agent, targets sterol synthesis in the pathogenic fungus Cryptococcus neoformans. Mol Microbiol 65: 1018-1033.
43. Lilly M, Bauer FF, Styger G, Lambrechts MG, Pretorius IS (2006) The effect of increased branched-chain amino acid transaminase activity in yeast on the production of higher alcohols and on the flavour profiles of wine and distillates. FEMS Yeast Res 6: 726-743.
44. Malavé TM, Dent SY (2006) Transcriptional repression by Tup1-Ssn6. Biochem Cell Biol 84: 437-443.
45. Martin T, Sherman DJ, Durrens P (2011) The Génolevures database. C R Biol 334: 585-589.
46. Masuo S, Terabayashi Y, Shimizu M, Fujii T, Kitazume T, Takaya N (2010) Global gene expression analysis of Aspergillus nidulans reveals metabolic shift and transcription suppression under hypoxia. Mol Genet Genomics 284: 415-424.
47. McA'Nulty MM, Whitehead JP, Lippard SJ (1996) Binding of Ixr1, a yeast HMG- domain protein, to cisplatin-DNA adducts in vitro and in vivo. Biochemistry 35: 6089-6099.
48. Melvin A, Rocha S (2012) Chromatin as an oxygen sensor and active player in the hypoxia response. Cell Signal 24: 35-43.
49. Mendes-Ferreira A, Barbosa C, Jiménez-Martí E, Del Olmo ML, Mendes-Faia A (2010) The wine yeast strain-dependent expression of genes implicated in sulfide production in response to nitrogen availability. J Microbiol Biotechnol 20: 1314-1321.
50. Merico A, Sulo P, Piškur J, Compagno C (2007) Fermentative lifestyle in yeasts belonging to the Saccharomyces complex. FEBS J 274(4): 976-989.
51. Merico A, Galafassi S, Piškur J, Compagno C (2009) The oxygen level determines the fermentation pattern in Kluyveromyces lactis. FEMS Yeast Res 9(5): 749-756.
52. Micolonghi C, Ottaviano D, Di Silvio E, Damato G, Heipieper H, Bianchi MM (2012) A dual signaling pathway for the hypoxic expression of lipid genes, dependent on the glucose sensor Rag4, is revealed by the analysis of KlMGA2 gene in Kluyveromyces lactis. Microbiology 158: 1734-1744.
53. Nakayama K (2009) Cellular signal transduction of the hypoxia response. J Biochem 146: 757-765.
54. Núñez L, Rodríguez-Torres A, Cerdán ME (2008) Regulatory elements in the KlHEM1 promoter. Biochim Biophys Acta 1779: 128-133.
55. Penacho V, Blondin B, Valero E, Gonzalez R (2012) Flocculation and transcriptional adaptation to fermentation conditions in a recombinant wine yeast strain defective for KNR4/SMI1. Biotechnol Prog 28: 327-336.
56. Poyton RO, Castello PR, Ball KA, Woo DK, Pan N (2009) Mitochondria and hypoxic signaling: a new view. Ann N Y Acad Sci 1177: 48-56.
57. Rodríguez Torres AM, Lamas Maceiras M, Rodríguez Belmonte E, Núñez Naveira L, Blanco Calvo M, Cerdán ME (2012) KlRox1p contributes to yeast resistance to metals and is necessary for KlYCF1 expression in the presence of cadmium. Gene 497: 27-37.
58. Setiadi ER, Doedt T, Cottier F, Noffz C, Ernst JF (2006) Transcriptional response of Candida albicans to hypoxia: linkage of oxygen sensing and Efg1p regulatory networks. J Mol Biol 361: 399-411.
59. Shimizu M, Fujii T, Masuo S, Fujita K, Takaya N (2009) Proteomic analysis of Aspergillus nidulans cultured under hypoxic conditions. Proteomics 9: 7-19.
60. Silva PA, Mussatto SI, Roberto IC, Teixeira JA (2010) Ethanol production from xylose by Pichia stipitis NRRLY-7124 in a stirred tank bioreactor. Brazilian J Chem Eng 28: 151-156.
61. Simeonidis E, Murabito E, Smallbone K, Westerhoff HV (2010) Why does yeast ferment? A flux balance analysis study. Biochem Soc Trans 38: 1225-1229.
62. Strogolova V, Furness A, Robb-McGrath M, Garlich J, Stuart RA (2012) Rcf1 and Rcf2, members of the hypoxia-induced gene 1 protein family, are critical components of the mitochondrial cytochrome bc1-cytochrome c oxidase supercomplex. Mol Cell Biol 32: 1363-1373.
63. Suzuki T, Yokoyama A, Tsuji T, Ikeshima E, Nakashima K, Ikushima S, Kobayashi C, Yoshida S (2011) Identification and characterization of genes involved in glutathione production in yeast. J Biosci Bioeng 112: 107-113.
64. Swiegers JH, Pretorius IS (2007) Modulation of volatile sulfur compounds by wine yeast. Appl Microbiol Biotechnol 74: 954-960.
65. Synnott JM, Guida A, Mulhern-Haughey S, Higgins DG, Butler G (2010) Regulation of the hypoxic response in Candida albicans. Eukaryot Cell 9: 1734-1746.
66. Tsaponina O, Barsoum E, Aström SU, Chabes A (2011) Ixr1 is required for the expression of the ribonucleotide reductase Rnr1 and maintenance of dNTP pools. PLoS Genet 7: e1002061.
67. Unrean P, Nguyen NA (2012) Metabolic pathway analysis of Scheffersomyces (Pichia) stipitis: effect of oxygen availability on ethanol synthesis and flux distributions. Appl Microbiol Biotechnol 94: 1387-1398.
68. Vizoso Vázquez A, Lamas Maceiras M, Becerra M, González Siso MI, Rodríguez Belmonte E, Cerdán ME (2012) Ixr1p and the control of the Saccharomyces cerevisiae hypoxic response. Appl Microbiol Biotechnol 94: 173-184.
69. Vukotic M, Oeljeklaus S, Wiese S, Vögtle FN, Meisinger C, Meyer HE, Zieseniss A, Katschinski DM, Jans DC, Jakobs S, Warscheid B, Rehling P, Deckers M (2012) Rcf1 mediates cytochrome oxidase assembly and respirasome formation, revealing heterogeneity of the enzyme complex. Cell Metab 15: 336-347.
70. Walker GM (1998) Yeast metabolism in "Yeast Physiology and Biotechnology". Wiley, Chichester.
71. Zara G, Angelozzi D, Belviso S, Bardi L, Goffrini P, Lodi T, Budroni M, Mannazzu I (2009) Oxygen is required to restore flor strain viability and lipid biosynthesis under fermentative conditions. FEMS Yeast Res 9: 217-225.