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High-affinity transport, cyanide-resistant respiration, and ethanol production under aerobiosis underlying efficient high glycerol consumption by Wickerhamomyces anomalus

  • Aureliano Claret da Cunha
  • Lorena Soares Gomes
  • Fernanda Godoy-Santos
  • Fábio Faria-Oliveira
  • Janaína Aparecida Teixeira
  • Geraldo Magela Santos Sampaio
  • Maria José Magalhães Trópia
  • Ieso Miranda Castro
  • Cândida Lucas
  • Rogelio Lopes BrandãoEmail author
Genetics and Molecular Biology of Industrial Organisms - Original Paper
  • 55 Downloads

Abstract

Wickerhamomyces anomalus strain LBCM1105 was originally isolated from the wort of cachaça (the Brazilian fermented sugarcane juice-derived Brazilian spirit) and has been shown to grow exceptionally well at high amounts of glycerol. This paramount residue from the biodiesel industry is a promising cheap carbon source for yeast biotechnology. The assessment of the physiological traits underlying the W. anomalus glycerol consumption ability in opposition to Saccharomyces cerevisiae is presented. A new WaStl1 concentrative glycerol-H+ symporter with twice the affinity of S. cerevisiae was identified. As in this yeast, WaSTL1 is repressed by glucose and derepressed/induced by glycerol but much more highly expressed. Moreover, LBCM1105 aerobically growing on glycerol was found to produce ethanol, providing a redox escape to compensate the redox imbalance at the level of cyanide-resistant respiration (CRR) and glycerol 3P shuttle. This work is critical for understanding the utilization of glycerol by non-Saccharomyces yeasts being indispensable to consider their industrial application feeding on biodiesel residue.

Keywords

Wickerhamomyces anomalus Glycerol metabolism Cachaça Biotechnological applications Glycerol transport STL1 

Notes

Acknowledgements

This work was supported by grants from Fundação de Capacitação de Pessoal de Nível Superior from the Ministry of Education—CAPES/Brazil (PNPD 2755/2011; PCF-PVE 021/2012), from FEDER through POFC-COMPETE and by FCT through strategic funding (UID/BIA/04050/2013), from Universidade Federal de Ouro Preto, and a research fellowship from Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (Brazil) Process 304815/2012 (research grant) and Process 305135/2015-5 (research fellowship to R.L.B.). C.L. is supported by the strategic program UID/BIA/04050/2013 [POCI-01-0145-FEDER-007569] funded by national funds through the FCT I.P. and by the ERDF through the COMPETE2020—Programa Operacional Competitividade e Internacionalização (POCI).The AUXPE-PVES 1801/2012 (Process 23038.015294/2016-18) from Brazilian Government supported a grant of Visiting Professor to C.L. and a research fellowships to A.C.C. and to F.F.O.

Compliance with ethical standards

Conflict of interest

Authors wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

References

  1. 1.
    Amaral PFF, Ferreira TF, Fontes GC, Coelho MAZ (2009) Glycerol valorization: new biotechnological routes. Food Bioprod Process 87:179–186.  https://doi.org/10.1016/j.fbp.2009.03.008 Google Scholar
  2. 2.
    Arous F, Atitallah IB, Nasri M, Mechichi T (2017) A sustainable use of low-cost raw substrates for biodiesel production by the oleaginous yeast Wickerhamomyces anomalus. 3 Biotech 7:268.  https://doi.org/10.1007/s13205-017-0903-6 Google Scholar
  3. 3.
    Ausubel FM, Struhl K, Smith JA, Seidman JG, Moore DD, Kingston RE, Brent R (1996) Current protocols in molecular biology. Wiley, New YorkGoogle Scholar
  4. 4.
    Barnett J, Yarrow D, Payne R, Barnett L (2000) Yeasts: characteristics and identification, 3rd edn. Cambridge University Press, Cambridge.  https://doi.org/10.1046/j.1525-1470.2001.1862020a.x Google Scholar
  5. 5.
  6. 6.
    Brasil (2016) Lei N. 13.263 - Altera a Lei nº 13.033, de 24 de setembro de 2014, para dispor sobre os percentuais de adição de biodiesel ao óleo diesel comercializado no território nacional. Brasília, Brasil http://www2.camara.leg.br/legin/fed/lei/2016/lei-13263-23-marco-2016-782625-publicacaooriginal-149818-pl.html
  7. 7.
    Buchan DW, Minneci F, Nugent TC, Bryson K, Jones DT (2013) Scalable web services for the PSIPRED protein analysis Workbench. Nucleic Acids Res 41:W349–W357.  https://doi.org/10.1093/nar/gkt381 Google Scholar
  8. 8.
    Clomburg JM, Gonzalez R (2013) Anaerobic fermentation of glycerol: a platform for renewable fuels and chemicals. Trends Biotechnol 31:20–28.  https://doi.org/10.1016/j.tibtech.2012.10.006 Google Scholar
  9. 9.
    da Conceicao LE, Saraiva MA, Diniz RH, Oliveira J, Barbosa GD, Alvarez F, Correa LF, Mezadri H, Coutrim MX, Afonso RJ, Lucas C, Castro IM, Brandao RL (2015) Biotechnological potential of yeast isolates from cachaça: the Brazilian spirit. J Ind Microbiol Biotechnol 42:237–246.  https://doi.org/10.1007/s10295-014-1528-y Google Scholar
  10. 10.
    DanielGietz R, Woods RA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. In: Guthrie C, Fink GR (eds) Methods in enzymology, vol 350. Academic Press, New York, pp 87–96.  https://doi.org/10.1016/S0076-6879(02)50957-5 Google Scholar
  11. 11.
    De Smidt O, Du Preez JC, Albertyn J (2008) The alcohol dehydrogenases of Saccharomyces cerevisiae: a comprehensive review. FEMS Yeast Res 8:967–978.  https://doi.org/10.1111/j.1567-1364.2008.00387.x Google Scholar
  12. 12.
    Díaz-Rincón DJ, Duque I, Osorio E, Rodríguez-López A, Espejo-Mojica A, Parra-Giraldo CM, Poutou-Piñales RA, Alméciga-Díaz CJ, Quevedo-Hidalgo B (2017) Production of recombinant Trichoderma reesei cellobiohydrolase II in a new expression system based on Wickerhamomyces anomalus. Enzyme Res 2017:6980565.  https://doi.org/10.1155/2017/6980565 Google Scholar
  13. 13.
    Duskova M, Ferreira C, Lucas C, Sychrova H (2015) Two glycerol uptake systems contribute to the high osmotolerance of Zygosaccharomyces rouxii. Mol Microbiol 97:541–559.  https://doi.org/10.1111/mmi.13048 Google Scholar
  14. 14.
    Ferreira C, Lucas C (2007) Glucose repression over Saccharomyces cerevisiae glycerol/H+ symporter gene STL1 is overcome by high temperature. FEBS Lett 581:1923–1927.  https://doi.org/10.1016/j.febslet.2007.03.086 Google Scholar
  15. 15.
    Ferreira C, van Voorst F, Martins A, Neves L, Oliveira R, Kielland-Brandt MC, Lucas C, Brandt A (2005) A member of the sugar transporter family, Stl1p is the glycerol/H+ symporter in Saccharomyces cerevisiae. Mol Biol Cell 16:2068–2076.  https://doi.org/10.1091/mbc.E04-10-0884 Google Scholar
  16. 16.
    Fredlund E, Druvefors U, Boysen ME, Lingsten KJ, Schnurer J (2002) Physiological characteristics of the biocontrol yeast Pichia anomala J121. FEMS Yeast Res 2:395–402.  https://doi.org/10.1111/j.1567-1364.2002.tb00109.x Google Scholar
  17. 17.
    Gao Z, Ma Y, Wang Q, Zhang M, Wang J, Liu Y (2016) Effect of crude glycerol impurities on lipid preparation by Rhodosporidium toruloides yeast 32489. Bioresour Technol 218:373–379.  https://doi.org/10.1016/j.biortech.2016.06.088 Google Scholar
  18. 18.
    González-Hernández J (2010) Molecular cloning and characterization of STL1 gene of Debaryomyces hansenii. J Yeast and Fungal Res 1(4):62–72Google Scholar
  19. 19.
    Guerra JB, Araujo RA, Pataro C, Franco GR, Moreira ES, Mendonca-Hagler LC, Rosa CA (2001) Genetic diversity of Saccharomyces cerevisiae strains during the 24 h fermentative cycle for the production of the artisanal Brazilian cachaça. Lett Appl Microbiol 33:106–111.  https://doi.org/10.1046/j.1472-765x.2001.00959.x Google Scholar
  20. 20.
    Ho PW, Klein M, Futschik M, Nevoigt E (2018) Glycerol positive promoters for tailored metabolic engineering of the yeast Saccharomyces cerevisiae. FEMS Yeast Res.  https://doi.org/10.1093/femsyr/foy019 Google Scholar
  21. 21.
    Hong SH, Song YS, Seo DJ, Kim KY, Jung WJ (2017) Antifungal activity and expression patterns of extracellular chitinase and beta-1,3-glucanase in Wickerhamomyces anomalus EG2 treated with chitin and glucan. Microb Pathog 110:159–164.  https://doi.org/10.1016/j.micpath.2017.06.038 Google Scholar
  22. 22.
    Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter MC, Rattei T, Mende DR, Sunagawa S, Kuhn M, Jensen LJ, von Mering C, Bork P (2016) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293.  https://doi.org/10.1093/nar/gkv1248 Google Scholar
  23. 23.
    IRENA (2014) A working paper for REmap 2030. Global bioenergy - supply and demand projections agency IRE, Abu Dhabi, United Arab Emirates http://www.irena.org/-/media/Files/IRENA/Agency/Publication/2014/IRENA_REmap_2030_Biomass_paper_2014.pdf
  24. 24.
    Kayingo G, Martins A, Andrie R, Neves L, Lucas C, Wong B (2009) A permease encoded by STL1 is required for active glycerol uptake by Candida albicans. Microbiology 155:1547–1557.  https://doi.org/10.1099/mic.0.023457-0 Google Scholar
  25. 25.
    Koutinas A, Vlysidis A, Pleissner D, Kopsahelis N, Lopez Garcia I, Kookos IK, Papanikolaou S, Kwan TH, Lin C (2014) Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers. Chem Soc Rev 43:2587–2627.  https://doi.org/10.1039/c3cs60293a Google Scholar
  26. 26.
    Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580.  https://doi.org/10.1006/jmbi.2000.4315 Google Scholar
  27. 27.
    Kurita O (2008) Increase of acetate ester-hydrolysing esterase activity in mixed cultures of Saccharomyces cerevisiae and Pichia anomala. J Appl Microbiol 104:1051–1058.  https://doi.org/10.1111/j.1365-2672.2007.03625.x Google Scholar
  28. 28.
    Lages F, Lucas C (1995) Characterization of a glycerol/H+ symport in the halotolerant yeast Pichia sorbitophila. Yeast 11:111–119.  https://doi.org/10.1002/yea.320110203 Google Scholar
  29. 29.
    Lages F, Lucas C (1997) Contribution to the physiological characterization of glycerol active uptake in Saccharomyces cerevisiae. Biochim Biophys Acta 1322:8–18Google Scholar
  30. 30.
    Lages F, Silva-Graca M, Lucas C (1999) Active glycerol uptake is a mechanism underlying halotolerance in yeasts: a study of 42 species. Microbiology 145(Pt 9):2577–2585.  https://doi.org/10.1099/00221287-145-9-2577 Google Scholar
  31. 31.
    Larsson C, Pahlman IL, Ansell R, Rigoulet M, Adler L, Gustafsson L (1998) The importance of the glycerol 3-phosphate shuttle during aerobic growth of Saccharomyces cerevisiae. Yeast 14:347–357.  https://doi.org/10.1002/(sici)1097-0061(19980315)14:4%3c347:aid-yea226%3e3.0.co;2-9 Google Scholar
  32. 32.
    Leiva-Candia DE, Tsakona S, Kopsahelis N, Garcia IL, Papanikolaou S, Dorado MP, Koutinas AA (2015) Biorefining of by-product streams from sunflower-based biodiesel production plants for integrated synthesis of microbial oil and value-added co-products. Bioresour Technol 190:57–65.  https://doi.org/10.1016/j.biortech.2015.03.114 Google Scholar
  33. 33.
    Leoneti AB, Aragão-Leoneti V, de Oliveira SVWB (2012) Glycerol as a by-product of biodiesel production in Brazil: alternatives for the use of unrefined glycerol. Renew Energy 45:138–145.  https://doi.org/10.1016/j.renene.2012.02.032 Google Scholar
  34. 34.
    Liu L-P, Zong M-H, Hu Y, Li N, Lou W-Y, Wu H (2017) Efficient microbial oil production on crude glycerol by Lipomyces starkeyi AS 2.1560 and its kinetics. Process Biochem (Oxford, UK) 58:230–238.  https://doi.org/10.1016/j.procbio.2017.03.024 Google Scholar
  35. 35.
    López V, Querol A, Ramón D, Fernández-Espinar MT (2001) A simplified procedure to analyse mitochondrial DNA from industrial yeasts. Int J Food Microbiol 68:75–81.  https://doi.org/10.1016/S0168-1605(01)00483-4 Google Scholar
  36. 36.
    Lucas C, Da Costa M, Van Uden N (1990) Osmoregulatory active sodium-glycerol co-transport in the halotolerant yeast Debaryomyces hansenii. Yeast 6:187–191.  https://doi.org/10.1002/yea.320060303 Google Scholar
  37. 37.
    Meher LC, Vidya Sagar D, Naik SN (2006) Technical aspects of biodiesel production by transesterification–a review. Renewable Sustainable Energy Rev 10:248–268.  https://doi.org/10.1016/j.rser.2004.09.002 Google Scholar
  38. 38.
    Melin P, Hakansson S, Eberhard TH, Schnurer J (2006) Survival of the biocontrol yeast Pichia anomala after long-term storage in liquid formulations at different temperatures, assessed by flow cytometry. J Appl Microbiol 100:264–271.  https://doi.org/10.1111/j.1365-2672.2005.02778.x Google Scholar
  39. 39.
    Merico A, Ragni E, Galafassi S, Popolo L, Compagno C (2011) Generation of an evolved Saccharomyces cerevisiae strain with a high freeze tolerance and an improved ability to grow on glycerol. J Ind Microbiol Biotechnol 38:1037–1044.  https://doi.org/10.1007/s10295-010-0878-3 Google Scholar
  40. 40.
    Minagawa N, Yoshimoto A (1987) The induction of cyanide-resistant respiration in Hansenula anomala. J Biochem 101:1141–1146Google Scholar
  41. 41.
    Mo EK, Sung CK (2014) Production of white pan bread leavened by Pichia anomala SKM-T. Food Sci Biotechnol 23:431–437.  https://doi.org/10.1007/s10068-014-0059-7 Google Scholar
  42. 42.
    Moore AL, Siedow JN (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059:121–140.  https://doi.org/10.1016/S0005-2728(05)80197-5 Google Scholar
  43. 43.
    Nevoigt E, Stahl U (1997) Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 21:231–241.  https://doi.org/10.1111/j.1574-6976.1997.tb00352.x Google Scholar
  44. 44.
    Niu C, Yuan Y, Hu Z, Wang Z, Liu B, Wang H, Yue T (2016) Accessing spoilage features of osmotolerant yeasts identified from kiwifruit plantation and processing environment in Shaanxi, China. Int J Food Microbiol 232:126–133.  https://doi.org/10.1016/j.ijfoodmicro.2016.03.012 Google Scholar
  45. 45.
    Ochoa-Estopier A, Lesage J, Gorret N, Guillouet SE (2011) Kinetic analysis of a Saccharomyces cerevisiae strain adapted for improved growth on glycerol: implications for the development of yeast bioprocesses on glycerol. Bioresour Technol 102:1521–1527.  https://doi.org/10.1016/j.biortech.2010.08.003 Google Scholar
  46. 46.
    OECD/FAO (2015) OECD-FAO agricultural outlook 2015. OECD Publishing, Paris.  https://doi.org/10.1787/agr_outlook-2015-en
  47. 47.
    Oleoline (2017) Glycerin market report. quarterly glycerine market report, Hong Kong. http://www.hbint.com/datas/media/590204fd077a6e381ef1a252/sample-quarterly-glycerine.pdf
  48. 48.
    Oliveira R, Lages F, Silva-Graca M, Lucas C (2003) Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. Biochim Biophys Acta 1613:57–71.  https://doi.org/10.1016/S0005-2736(03)00138-X Google Scholar
  49. 49.
    Oro L, Feliziani E, Ciani M, Romanazzi G, Comitini F (2018) Volatile organic compounds from Wickerhamomyces anomalus, Metschnikowia pulcherrima and Saccharomyces cerevisiae inhibit growth of decay causing fungi and control postharvest diseases of strawberries. Int J Food Microbiol 265:18–22.  https://doi.org/10.1016/j.ijfoodmicro.2017.10.027 Google Scholar
  50. 50.
    Passoth V, Fredlund E, Druvefors UA, Schnurer J (2006) Biotechnology, physiology and genetics of the yeast Pichia anomala. FEMS Yeast Res 6:3–13.  https://doi.org/10.1111/j.1567-1364.2005.00004.x Google Scholar
  51. 51.
    Pereira I, Madeira A, Prista C, Loureiro-Dias MC, Leandro MJ (2014) Characterization of new polyol/H+ symporters in Debaryomyces hansenii. PLoS ONE 9:e88180.  https://doi.org/10.1371/journal.pone.0088180 Google Scholar
  52. 52.
    Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.  https://doi.org/10.1093/nar/29.9.e45 Google Scholar
  53. 53.
    Riley R, Haridas S, Wolfe KH, Lopes MR, Hittinger CT, Goker M, Salamov AA, Wisecaver JH, Long TM, Calvey CH, Aerts AL, Barry KW, Choi C, Clum A, Coughlan AY, Deshpande S, Douglass AP, Hanson SJ, Klenk HP, LaButti KM, Lapidus A, Lindquist EA, Lipzen AM, Meier-Kolthoff JP, Ohm RA, Otillar RP, Pangilinan JL, Peng Y, Rokas A, Rosa CA, Scheuner C, Sibirny AA, Slot JC, Stielow JB, Sun H, Kurtzman CP, Blackwell M, Grigoriev IV, Jeffries TW (2016) Comparative genomics of biotechnologically important yeasts. Proc Natl Acad Sci U S A 113:9882–9887.  https://doi.org/10.1073/pnas.1603941113 Google Scholar
  54. 54.
    Saier MH (1999) Eukaryotic transmembrane solute transport systems. In: Jeon KW (ed) International review of cytology, vol 190. Academic Press, New York, pp 61-136.  https://doi.org/10.1016/S0074-7696(08)62146-4
  55. 55.
    Sakajo S, Minagawa N, Yoshimoto A (1993) Characterization of the alternative oxidase protein in the yeast Hansenula anomala. FEBS Lett 318:310–312.  https://doi.org/10.1016/0014-5793(93)80535-3 Google Scholar
  56. 56.
    Sakajo S, Minagawa N, Yoshimoto A (1999) Structure and regulatory expression of a single copy alternative oxidase gene from the yeast Pichia anomala. Biosci Biotechnol Biochem 63:1889–1894.  https://doi.org/10.1271/bbb.63.1889 Google Scholar
  57. 57.
    Schneider J, Rupp O, Trost E, Jaenicke S, Passoth V, Goesmann A, Tauch A, Brinkrolf K (2012) Genome sequence of Wickerhamomyces anomalus DSM 6766 reveals genetic basis of biotechnologically important antimicrobial activities. FEMS Yeast Res 12:382–386.  https://doi.org/10.1111/j.1567-1364.2012.00791.x Google Scholar
  58. 58.
    Sherman F (2002) Getting started with yeast. In: Guthrie C, Fink GR (eds) Methods in enzymology, vol 350. Academic Press, New York, pp 3-41.  https://doi.org/10.1016/S0076-6879(02)50954-X
  59. 59.
    Siderius M, Van Wuytswinkel O, Reijenga KA, Kelders M, Mager WH (2000) The control of intracellular glycerol in Saccharomyces cerevisiae influences osmotic stress response and resistance to increased temperature. Mol Microbiol 36:1381–1390.  https://doi.org/10.1046/j.1365-2958.2000.01955.x Google Scholar
  60. 60.
    Singh MV, Anthony Weil P (2002) A method for plasmid purification directly from yeast. Anal Biochem 307:13–17.  https://doi.org/10.1016/S0003-2697(02)00018-0 Google Scholar
  61. 61.
    Souza KS, Ramos CL, Schwan RF, Dias DR (2017) Lipid production by yeasts grown on crude glycerol from biodiesel industry. Prep Biochem Biotechnol 47:357–363.  https://doi.org/10.1080/10826068.2016.1244689 Google Scholar
  62. 62.
    Souza KST, Gudina EJ, Azevedo Z, de Freitas V, Schwan RF, Rodrigues LR, Dias DR, Teixeira JA (2017) New glycolipid biosurfactants produced by the yeast strain Wickerhamomyces anomalus CCMA 0358. Colloids Surf B 154:373–382.  https://doi.org/10.1016/j.colsurfb.2017.03.041 Google Scholar
  63. 63.
    Spier F, Buffon JG, Burkert CAV (2015) Bioconversion of raw glycerol generated from the synthesis of biodiesel by different oleaginous yeasts: lipid content and fatty acid profile of biomass. Indian J Microbiol 55:415–422.  https://doi.org/10.1007/s12088-015-0533-9 Google Scholar
  64. 64.
    Swinnen S, Ho PW, Klein M, Nevoigt E (2016) Genetic determinants for enhanced glycerol growth of Saccharomyces cerevisiae. Metab Eng 36:68–79.  https://doi.org/10.1016/j.ymben.2016.03.003 Google Scholar
  65. 65.
    Swinnen S, Klein M, Carrillo M, McInnes J, Nguyen HTT, Nevoigt E (2013) Re-evaluation of glycerol utilization in Saccharomyces cerevisiae: characterization of an isolate that grows on glycerol without supporting supplements. Biotechnol Biofuels 6:157.  https://doi.org/10.1186/1754-6834-6-157 Google Scholar
  66. 66.
    Thomik T, Wittig I, Choe JY, Boles E, Oreb M (2017) An artificial transport metabolon facilitates improved substrate utilization in yeast. Nat Chem Biol 13:1158–1163.  https://doi.org/10.1038/nchembio.2457 Google Scholar
  67. 67.
    Tulha J, Carvalho J, Armada R, Faria-Oliveira F, Lucas C, Pais C, Almeida J, Ferreira C (2012) Yeast, the man’s best friend. In: Benjamin Valdez RZ, Schorr M (ed) Scientific, health and social aspects of the food industry. INTECH Open Access Publisher, Instituto de Ingeniería, Universidad Autónoma de Baja California, Mexicali, México.  https://doi.org/10.5772/31471
  68. 68.
    Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics (Oxford, England) 17:849–850Google Scholar
  69. 69.
    Veiga A, Arrabaca JD, Loureiro-Dias MC (2000) Cyanide-resistant respiration is frequent, but confined to yeasts incapable of aerobic fermentation. FEMS Microbiol Lett 190:93–97.  https://doi.org/10.1111/j.1574-6968.2000.tb09268.x Google Scholar
  70. 70.
    Vickers CE, Bydder SF, Zhou Y, Nielsen LK (2013) Dual gene expression cassette vectors with antibiotic selection markers for engineering in Saccharomyces cerevisiae. Microb Cell Fact 12:96.  https://doi.org/10.1186/1475-2859-12-96 Google Scholar
  71. 71.
    Wahyono A, Kang W-W, H-d Park (2015) Characterization and application of Torulaspora delbrueckii JK08 and Pichia anomala JK04 as baker’s yeasts. J Food Nutr Res (Bratislava, Slovakia) 54:205–207Google Scholar
  72. 72.
    Wallace-Salinas V, Signori L, Li Y-Y, Ask M, Bettiga M, Porro D, Thevelein JM, Branduardi P, Foulquié-Moreno MR, Gorwa-Grauslund M (2014) Re-assessment of YAP1 and MCR1 contributions to inhibitor tolerance in robust engineered Saccharomyces cerevisiae fermenting undetoxified lignocellulosic hydrolysate. AMB Express 4:56.  https://doi.org/10.1186/s13568-014-0056-5 Google Scholar
  73. 73.
    Wojda I, Alonso-Monge R, Bebelman JP, Mager WH, Siderius M (2003) Response to high osmotic conditions and elevated temperature in Saccharomyces cerevisiae is controlled by intracellular glycerol and involves coordinate activity of MAP kinase pathways. Microbiology 149:1193–1204.  https://doi.org/10.1099/mic.0.26110-0 Google Scholar
  74. 74.
    Yachdav G, Kloppmann E, Kajan L, Hecht M, Goldberg T, Hamp T, Honigschmid P, Schafferhans A, Roos M, Bernhofer M, Richter L, Ashkenazy H, Punta M, Schlessinger A, Bromberg Y, Schneider R, Vriend G, Sander C, Ben-Tal N, Rost B (2014) PredictProtein—an open resource for online prediction of protein structural and functional features. Nucleic Acids Res 42:W337–W343.  https://doi.org/10.1093/nar/gku366 Google Scholar
  75. 75.
    Yazdani SS, Gonzalez R (2007) Anaerobic fermentation of glycerol: a path to economic viability for the biofuels industry. Curr Opin Biotechnol 18:213–219.  https://doi.org/10.1016/j.copbio.2007.05.002 Google Scholar
  76. 76.
    Zimmermann L, Stephens A, Nam SZ, Rau D, Kubler J, Lozajic M, Gabler F, Soding J, Lupas AN, Alva V (2017) A completely reimplemented MPI bioinformatics toolkit with a new HHpred server at its core. J Mol Biol.  https://doi.org/10.1016/j.jmb.2017.12.007

Copyright information

© Society for Industrial Microbiology and Biotechnology 2019

Authors and Affiliations

  • Aureliano Claret da Cunha
    • 1
  • Lorena Soares Gomes
    • 1
  • Fernanda Godoy-Santos
    • 1
  • Fábio Faria-Oliveira
    • 1
  • Janaína Aparecida Teixeira
    • 1
  • Geraldo Magela Santos Sampaio
    • 1
  • Maria José Magalhães Trópia
    • 1
  • Ieso Miranda Castro
    • 1
  • Cândida Lucas
    • 2
  • Rogelio Lopes Brandão
    • 1
    Email author
  1. 1.Laboratório de Biologia Celular e MolecularNUPEB, Universidade Federal de Ouro PretoOuro PretoBrazil
  2. 2.Instituto de Ciência e Inovação em Bio-Sustentabilidade (IB-S)/Centro de Biologia Molecular e Ambiental (CBMA)Universidade do MinhoBragaPortugal

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