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

  • Genetics and Molecular Biology of Industrial Organisms - Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

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.

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References

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ausubel FM, Struhl K, Smith JA, Seidman JG, Moore DD, Kingston RE, Brent R (1996) Current protocols in molecular biology. Wiley, New York

    Google Scholar 

  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

    Book  Google Scholar 

  5. Brasil (2013) Plano Decenal de Expansão de Energia. Brasília, Brasil http://www.epe.gov.br/sites-pt/publicacoes-dados-abertos/publicacoes/PublicacoesArquivos/publicacao-49/topico-86/Relat%C3%B3rio%20Final%20do%20PDE%202022.pdf

  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. 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

    Article  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Chapter  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  18. González-Hernández J (2010) Molecular cloning and characterization of STL1 gene of Debaryomyces hansenii. J Yeast and Fungal Res 1(4):62–72

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  29. Lages F, Lucas C (1997) Contribution to the physiological characterization of glycerol active uptake in Saccharomyces cerevisiae. Biochim Biophys Acta 1322:8–18

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  40. Minagawa N, Yoshimoto A (1987) The induction of cyanide-resistant respiration in Hansenula anomala. J Biochem 101:1141–1146

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  46. OECD/FAO (2015) OECD-FAO agricultural outlook 2015. OECD Publishing, Paris. https://doi.org/10.1787/agr_outlook-2015-en

  47. Oleoline (2017) Glycerin market report. quarterly glycerine market report, Hong Kong. http://www.hbint.com/datas/media/590204fd077a6e381ef1a252/sample-quarterly-glycerine.pdf

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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. 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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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. 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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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. Tusnady GE, Simon I (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics (Oxford, England) 17:849–850

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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) 54:205–207

    CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

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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.

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  1. Laboratório de Biologia Celular e Molecular, NUPEB, Universidade Federal de Ouro Preto, Campus do Morro do Cruzeiro, Ouro Preto, MG, 35.400-000, Brazil

    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 & Rogelio Lopes Brandão

  2. Instituto de Ciência e Inovação em Bio-Sustentabilidade (IB-S)/Centro de Biologia Molecular e Ambiental (CBMA), Universidade do Minho, Braga, Portugal

    Cândida Lucas

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Correspondence to Rogelio Lopes Brandão.

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da Cunha, A.C., Gomes, L.S., Godoy-Santos, F. et al. High-affinity transport, cyanide-resistant respiration, and ethanol production under aerobiosis underlying efficient high glycerol consumption by Wickerhamomyces anomalus. J Ind Microbiol Biotechnol 46, 709–723 (2019). https://doi.org/10.1007/s10295-018-02119-5

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