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Applied Microbiology and Biotechnology

, Volume 102, Issue 5, pp 2101–2116 | Cite as

Anaerobiosis revisited: growth of Saccharomyces cerevisiae under extremely low oxygen availability

  • Bruno Labate Vale da Costa
  • Thiago Olitta Basso
  • Vijayendran Raghavendran
  • Andreas Karoly Gombert
Mini-Review

Abstract

The budding yeast Saccharomyces cerevisiae plays an important role in biotechnological applications, ranging from fuel ethanol to recombinant protein production. It is also a model organism for studies on cell physiology and genetic regulation. Its ability to grow under anaerobic conditions is of interest in many industrial applications. Unlike industrial bioreactors with their low surface area relative to volume, ensuring a complete anaerobic atmosphere during microbial cultivations in the laboratory is rather difficult. Tiny amounts of O2 that enter the system can vastly influence product yields and microbial physiology. A common procedure in the laboratory is to sparge the culture vessel with ultrapure N2 gas; together with the use of butyl rubber stoppers and norprene tubing, O2 diffusion into the system can be strongly minimized. With insights from some studies conducted in our laboratory, we explore the question ‘how anaerobic is anaerobiosis?’. We briefly discuss the role of O2 in non-respiratory pathways in S. cerevisiae and provide a systematic survey of the attempts made thus far to cultivate yeast under anaerobic conditions. We conclude that very few data exist on the physiology of S. cerevisiae under anaerobiosis in the absence of the anaerobic growth factors ergosterol and unsaturated fatty acids. Anaerobicity should be treated as a relative condition since complete anaerobiosis is hardly achievable in the laboratory. Ideally, researchers should provide all the details of their anaerobic set-up, to ensure reproducibility of results among different laboratories.

Keywords

Anaerobiosis Oxygen Saccharomyces cerevisiae Chemostat cultivation Anaerobic growth factors 

Notes

Funding information

This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, São Paulo, Brazil), through grant number 2015/14109-0, and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brasília, Brazil) through a PNPD grant to VR and a Ph.D. scholarship to BLVC. The authors would like to thank the faculty and the staff from the Department of Chemical Engineering, University of São Paulo, for allowing us to use their infra-structure and equipment for the experimental work.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Aceituno FF, Orellana M, Torres J, Mendoza S, Slater AW, Melo F, Agosin E (2012) Oxygen response of the wine yeast Saccharomyces cerevisiae EC1118 grown under carbon-sufficient, nitrogen-limited enological conditions. Appl Environ Microbiol 78(23):8340–8352.  https://doi.org/10.1128/aem.02305-12 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alterthum F, Rose AH (1973) Osmotic lysis of sphaeroplasts from Saccharomyces cerevisiae grown anaerobically in media containing different unsaturated fatty acids. J Gen Microbiol 77(2):371–382.  https://doi.org/10.1099/00221287-77-2-371 CrossRefPubMedGoogle Scholar
  3. Andreasen AA, Stier TJB (1953) Anaerobic nutrition of Saccharomyces cerevisiae. I Ergosterol requirement for growth in a defined medium. J Cell Compar Physl 41(1):23–36.  https://doi.org/10.1002/jcp.1030410103 CrossRefGoogle Scholar
  4. Andreasen AA, Stier TJB (1954) Anaerobic nutrition of Saccharomyces cerevisiae. II Unsaturated fatty acid requirement for growth in a defined medium. J Cell Compar Physl 43(3):271–281.  https://doi.org/10.1002/jcp.1030430303 CrossRefGoogle Scholar
  5. Aries V, Kirsop BH (1977) Sterol synthesis in relation to growth and fermentation by brewing yeasts inoculated at different concentrations. J I Brewing 83(4):220–223.  https://doi.org/10.1002/j.2050-0416.1977.tb03798.x CrossRefGoogle Scholar
  6. Balch WE, Wolfe RS (1976) New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressureized atmosphere. Appl Environ Microbiol 32(6):781–791PubMedPubMedCentralGoogle Scholar
  7. Barnett JA (2003) A history of research on yeasts 5: the fermentation pathway. Yeast 20(6):509–543.  https://doi.org/10.1002/yea.986 CrossRefPubMedGoogle Scholar
  8. Bieglmayer C, Ruis H (1977) A simple fermentor for growth of strictly anaerobic yeast in small volumes. Anal Biochem 83(1):322–325.  https://doi.org/10.1016/0003-2697(77)90543-7 CrossRefPubMedGoogle Scholar
  9. Bisschops M, Vos T, Martinez-Moreno R, de la Torre Cortes P, Pronk J, Daran-Lapujade P (2015) Oxygen availability strongly affects chronological lifespan and thermotolerance in batch cultures of Saccharomyces cerevisiae. Microb Cell 2:429–444.  https://doi.org/10.15698/mic2015.11.238 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Boender LGM, de Hulster EAF, Van Maris AJA, Pronk JT, Daran-Lapujade P (2009) Quantitative physiology of Saccharomyces cerevisiae at near-zero specific growth rates. Appl Environ Microbiol 75(17):5607–5614.  https://doi.org/10.1128/AEM.00429-09 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Börner RA (2016) Isolation and cultivation of anaerobes. In: Hatti-Kaul R, Mamo G, Mattiasson B (eds) Anaerobes in biotechnology. Springer, Cham, pp 35–53.  https://doi.org/10.1007/10_2016_1 CrossRefGoogle Scholar
  12. Bragger JM, Daniel RM, Coolbear T, Morgan HW (1989) Very stable enzymes from extremely thermophilic archaebacteria and eubacteria. Appl Microbiol Biotechnol 31-31(5-6):556–561.  https://doi.org/10.1007/BF00270794 CrossRefGoogle Scholar
  13. Brewer JH, Allgeier DL, McLaughlin CB (1966) Improved anaerobic indicator. Appl Microbiol 14(1):135–136PubMedPubMedCentralGoogle Scholar
  14. Brockmann MC, Stier TJB (1947) Steady state fermentation by yeast in a growth medium. J Cell Compar Physl 29(1):1–14.  https://doi.org/10.1002/jcp.1030290102 CrossRefGoogle Scholar
  15. Bryant MP (1972) Commentary on the Hungate technique for culture of anaerobic bacteria. Am J Clin Nutr 25(12):1324–1328CrossRefPubMedGoogle Scholar
  16. Burke PV, Kwast KE, Everts F, Poyton RO (1998) A fermentor system for regulating oxygen at low concentrations in cultures of Saccharomyces cerevisiae. Appl Environ Microbiol 64(3):1040–1044PubMedPubMedCentralGoogle Scholar
  17. Burke PV, Raitt DC, Allen LA, Kellogg EA, Poyton RO (1997) Effects of oxygen concentration on the expression of cytochrome c and cytochrome c oxidase genes in yeast. J Biol Chem 272(23):14705–14712.  https://doi.org/10.1074/jbc.272.23.14705 CrossRefPubMedGoogle Scholar
  18. Ceccarelli EA, Rosano GL (2014) Recombinant protein expression in microbial systems. Frontiers E-booksGoogle Scholar
  19. Coy (1969) Laboratory Products, Inc, USA. In: https://coylab.com. https://coylab.com/company/. Accessed 8 Oct 2017
  20. Curran JS, Smith J, Holms W (1989) Heat-and-power in industrial fermentation processes. Appl Energ 34(1):9–20.  https://doi.org/10.1016/0306-2619(89)90051-2 CrossRefGoogle Scholar
  21. Dagsgaard C, Taylor LE, O’Brien KM, Poyton RO (2001) Effects of anoxia and the mitochondrion on expression of aerobic nuclear COX genes in yeast: evidence for a signaling pathway from the mitochondrial genome to the nucleus. J Biol Chem 276(10):7593–7601.  https://doi.org/10.1074/jbc.M009180200 CrossRefPubMedGoogle Scholar
  22. Daniels L, Zeikus JG (1975) Improved culture flask for obligate anaerobes. Appl Microbiol 29(5):710–711PubMedPubMedCentralGoogle Scholar
  23. Daum G, Lees ND, Bard M, Dickson R (1998) Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast 14(16):1471–1510.  https://doi.org/10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y CrossRefPubMedGoogle Scholar
  24. David LA, Alm EJ (2011) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469(7328):93–96.  https://doi.org/10.1038/nature09649 CrossRefPubMedGoogle Scholar
  25. David MH, Kirsop BH (2013) Yeast growth in relation to the dissolved oxygen and sterol content of worth. J I Brewing 79(1):20–25.  https://doi.org/10.1002/j.2050-0416.1973.tb03491.x CrossRefGoogle Scholar
  26. de Becze G, Liebmann AJ (1944) Aeration in the production of compressed yeast. Ind Eng Chem 36(10):882–890.  https://doi.org/10.1021/ie50418a004 CrossRefGoogle Scholar
  27. de Kok S, Yilmaz D, Suir E, Pronk JT, van Maris AJ, Daran JM (2011) Increasing free-energy (ATP) conservation in maltose-grown Saccharomyces cerevisiae by expression of a heterologous maltose phosphorylase. Metab Eng 13(5):518–526.  https://doi.org/10.1016/j.ymben.2011.06.001 CrossRefPubMedGoogle Scholar
  28. Della-Bianca BE, Basso TO, Stambuk BU, Basso LC, Gombert AK (2013) What do we know about the yeast strains from the Brazilian fuel ethanol industry? Appl Microbiol Biotechnol 97(3):979–991.  https://doi.org/10.1007/s00253-012-4631-x CrossRefPubMedGoogle Scholar
  29. Denny MW (1993) Air and water. Princeton University PressGoogle Scholar
  30. Dobson PD, Smallbone K, Jameson D, Simeonidis E, Lanthaler K, Pir P, Lu C, Swainston N, Dunn WB, Fisher P, Hull D, Brown M, Oshota O, Stanford NJ, Kell DB, King RD, Oliver SG, Stevens RD, Mendes P (2010) Further developments towards a genome-scale metabolic model of yeast. BMC Syst Biol 4(1):145.  https://doi.org/10.1186/1752-0509-4-145 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fornairon-Bonnefond C, Demaretz V, Rosenfeld E, Salmon J-M (2002) Oxygen addition and sterol synthesis in Saccharomyces cerevisiae during enological fermentation. J Biosci Bioeng 93(2):176–182.  https://doi.org/10.1016/S1389-1723(02)80011-1 CrossRefPubMedGoogle Scholar
  32. Garcia-Ochoa F, Gomez E, Santos VE, Merchuk JC (2010) Oxygen uptake rate in microbial processes: an overview. Biochem Eng J 49(3):289–307.  https://doi.org/10.1016/j.bej.2010.01.011 CrossRefGoogle Scholar
  33. Gest H (2004) The discovery of microorganisms by Robert Hooke and Antoni van Leeuwenhoek, fellows of the Royal Society. Notes Rec R Soc Lond 58(2):187–201.  https://doi.org/10.1098/rsnr.2004.0055 CrossRefPubMedGoogle Scholar
  34. Giacobbe FW (1990) Oxygen permeability of teflon–PFA tubing. J Appl Poly Sci 39(5):1121–1132.  https://doi.org/10.1002/app.1990.070390508 CrossRefGoogle Scholar
  35. Gordon JH, Dubos R (1970) The anaerobic bacterial flora of the mouse cecum. J Exp Med 132(2):251–260.  https://doi.org/10.1084/jem.132.2.251 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hall IC (1929) A review of the development and application of physical and chemical principles in the cultivation of obligately anaerobic bacteria. J Bacteriol 17(4):255–301PubMedPubMedCentralGoogle Scholar
  37. Hanotu J, Kong D, Zimmerman WB (2016) Intensification of yeast production with microbubbles. Food Bioprod Process 100:424–431.  https://doi.org/10.1016/j.fbp.2016.07.013 CrossRefGoogle Scholar
  38. Hatti-Kaul R, Mattiasson B (2016) Anaerobes in industrial- and environmental biotechnology. In: Hatti-Kaul R, Mamo G, Mattiasson B (eds) Anaerobes in biotechnology. Springer International Publishing, pp 1–33Google Scholar
  39. Heavner BD, Smallbone K, Barker B, Mendes P, Walker LP (2012) Yeast 5—an expanded reconstruction of the Saccharomyces cerevisiae metabolic network. BMC Syst Biol 6(1):55.  https://doi.org/10.1186/1752-0509-6-55 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Herrgård MJ, Swainston N, Dobson PD, Dunn WB, Arga KY, Arvas M, Bluthgen N, Borger S, Costenoble R, Heinemann M, Hucka M, Le Novere N, Li P, Liebermeister W, Mo ML, Oliveira AP, Petranovic D, Pettifer S, Simeonidis E, Smallbone K, Spasic I, Weichart D, Brent R, Broomhead DS, Westerhoff HV, Kirdar B, Penttila M, Klipp E, Palsson BO, Sauer U, Oliver SG, Mendes P, Nielsen J, Kell DB (2008) A consensus yeast metabolic network reconstruction obtained from a community approach to systems biology. Nat Biotechnol 26(10):1155–1160.  https://doi.org/10.1038/nbt1492 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Huerta-Sanchez E, Jin X, Asan, Bianba Z, Peter BM, Vinckenbosch N, Liang Y, Yi X, He M, Somel M, Ni P, Wang B, Ou X, Huasang LJ, Cuo ZXP, Li K, Gao G, Yin Y, Wang W, Zhang X, Xu X, Yang H, Li Y, Wang J, Wang J, Nielsen R (2014) Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512:194.  https://doi.org/10.1038/nature13408 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hungate RE (1969) A roll tube method for cultivation of strict anaerobes. In: Methods in microbiology. Elsevier, pp 117–132Google Scholar
  43. Imlay JA (2008) How obligatory is anaerobiosis? Mol Microbiol 68(4):801–804.  https://doi.org/10.1111/j.1365-2958.2008.06213.x CrossRefPubMedPubMedCentralGoogle Scholar
  44. Jeon BS, Choi O, Um Y, Sang B-I (2016) Production of medium-chain carboxylic acids by Megasphaera sp. MH with supplemental electron acceptors. Biotechnol Biofuels 9(1):129.  https://doi.org/10.1186/s13068-016-0549-3 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Jollow D, Kellerman GM, Linnane AW (1968) The biogenesis of mitochondria. III. The lipid composition of aerobically and anaerobically grown Saccharomyces cerevisiae as related to the membrane systems of the cells. J Cell Biol 37(2):221–230.  https://doi.org/10.1083/jcb.37.2.221 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Jouhten P, Penttilä M (2014) Anaerobic carbon metabolism of Saccharomyces cerevisiae. In: Piškur J, Compagno C (eds) Molecular mechanisms in yeast carbon metabolism (eBook). Springer, Berlin Heidelberg, pp 57–82CrossRefGoogle Scholar
  47. Jouhten P, Rintala E, Huuskonen A, Tamminen A, Toivari M, Wiebe M, Ruohonen L, Penttilä M, Maaheimo H (2008) Oxygen dependence of metabolic fluxes and energy generation of Saccharomyces cerevisiae CEN.PK113-1A. BMC Syst Biol 2(1):60.  https://doi.org/10.1186/1752-0509-2-60 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Jouhten P, Wiebe M, Penttilä M (2012) Dynamic flux balance analysis of the metabolism of Saccharomyces cerevisiae during the shift from fully respirative or respirofermentative metabolic states to anaerobiosis. FEBS J 279(18):3338–3354.  https://doi.org/10.1111/j.1742-4658.2012.08649.x CrossRefPubMedGoogle Scholar
  49. Kato MT, Field JA, Lettinga G (1997) Anaerobe tolerance to oxygen and the potentials of anaerobic and aerobic cocultures for wastewater treatment. Braz J Chem Eng 14(4):395–407.  https://doi.org/10.1590/s0104-66321997000400015 CrossRefGoogle Scholar
  50. Kawasaki S, Watamura Y, Ono M, Watanabe T, Takeda K, Niimura Y (2005) Adaptive responses to oxygen stress in obligatory anaerobes Clostridium acetobutylicum and Clostridium aminovalericum. Appl Environ Microbiol 71(12):8442–8450.  https://doi.org/10.1128/AEM.71.12.8442-8450.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Kiers J, Zeeman A-M, Luttik M, Thiele C, Castrillo JI, Steensma HY, van Dijken JP, Pronk JT (1998) Regulation of alcoholic fermentation in batch and chemostat cultures of Kluyveromyces lactis CBS 2359. Yeast 14(5):459–469.  https://doi.org/10.1002/(SICI)1097-0061(19980330)14:5<459::AID-YEA248>3.0.CO;2-O CrossRefPubMedGoogle Scholar
  52. Klose C, Surma MA, Gerl MJ, Meyenhofer F, Shevchenko A, Simons K (2012) Flexibility of a eukaryotic lipidome – insights from yeast lipidomics. PLoS One 7(4):e35063.  https://doi.org/10.1371/journal.pone.0035063 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kováč L, Subík J, Russ G, Kollár K (1967) On the relationship between respiratory activity and lipid composition of the yeast cell. BBA-Bioenergetics 144(1):94–101PubMedGoogle Scholar
  54. Köpke M, Gerth ML, Maddock DJ, Mueller AP, Liew F, Simpson SD, Patrick WM (2014) Reconstruction of an acetogenic 2,3-butanediol pathway involving a novel NADPH-dependent primary-secondary alcohol dehydrogenase. Appl Environ Microbiol 80(11):3394–3403.  https://doi.org/10.1128/AEM.00301-14 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kwast KE, Lai L-C, Menda N, James DT, Aref S, Burke PV (2002) Genomic analyses of anaerobically induced genes in Saccharomyces cerevisiae: functional roles of Rox1 and other factors in mediating the anoxic response. J Bacteriol 184(1):250–265.  https://doi.org/10.1128/JB.184.1.250-265.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lane N (2002) Oxygen: the molecule that made the world. OUP OxfordGoogle Scholar
  57. Lane N, Martin W (2010) The energetics of genome complexity. Nature 467(7318):929–934.  https://doi.org/10.1038/nature09486 CrossRefPubMedGoogle Scholar
  58. Lindberg L, Santos AX, Riezman H, Olsson L, Bettiga M (2013) Lipidomic profiling of Saccharomyces cerevisiae and Zygosaccharomyces bailii reveals critical changes in lipid composition in response to acetic acid stress. PLoS One 8(9):e73936.  https://doi.org/10.1371/journal.pone.0073936 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Linde t JJ, Liang H, Davis RW, Steensma HY, van Dijken JP, Pronk JT (1999) Genome-wide transcriptional analysis of aerobic and anaerobic chemostat cultures of Saccharomyces cerevisiae. J Bacteriol 181:7409–7413PubMedPubMedCentralGoogle Scholar
  60. Littlechild JA (2015) Archaeal enzymes and applications in industrial biocatalysts. Archaea 2015(10):1–10.  https://doi.org/10.1155/2015/147671 CrossRefGoogle Scholar
  61. Macy JM, Miller MW (1983) Anaerobic growth of Saccharomyces cerevisiae in the absence of oleic acid and ergosterol? Arch Microbiol 134(1):64–67.  https://doi.org/10.1007/BF00429409 CrossRefGoogle Scholar
  62. Masterflex® (2017) pump tubing formulation descriptions. In: masterflex.be. http://www.masterflex.be/Downloads/masterflex_slangmaterialen.pdf. Accessed 8 Oct 2017
  63. Maw GA (1961) Effects of cysteine and other thiols on the growth of a brewer’s yeast. J I Brewing 67(1):57–63.  https://doi.org/10.1002/j.2050-0416.1961.tb01759.x CrossRefGoogle Scholar
  64. Meites L, Meltes T (1948) Removal of oxygen from gas streams. Anal Chem 20(10):984–985.  https://doi.org/10.1021/ac60022a044 CrossRefGoogle Scholar
  65. Merico A, Galafassi S, Piskur J, Compagno C (2009) The oxygen level determines the fermentation pattern in Kluyveromyces lactis. FEMS Yeast Res 9(5):749–756.  https://doi.org/10.1111/j.1567-1364.2009.00528.x CrossRefPubMedGoogle Scholar
  66. Merico A, Sulo P, Piškur J, Compagno C (2007) Fermentative lifestyle in yeasts belonging to the Saccharomyces complex. FEBS J 274(4):976–989.  https://doi.org/10.1111/j.1742-4658.2007.05645.x CrossRefPubMedGoogle Scholar
  67. Miller TL, Wolin MJ (1974) A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 27(5):985–987PubMedPubMedCentralGoogle Scholar
  68. Nakagawa Y, Sugioka S, Kaneko Y, Harashima S (2001) O2R, a novel regulatory element mediating Rox1p-independent O2 and unsaturated fatty acid repression of OLE1 in Saccharomyces cerevisiae. J Bacteriol 183(2):745–751.  https://doi.org/10.1128/JB.183.2.745-751.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Navas-Iglesias N, Carrasco-Pancorbo A, Cuadros-Rodríguez L (2009) From lipids analysis towards lipidomics, a new challenge for the analytical chemistry of the 21st century. Part II: analytical lipidomics. TrAC-Trend Anal Chem 28(4):393–403.  https://doi.org/10.1016/j.trac.2008.12.004 CrossRefGoogle Scholar
  70. O’Brien RW, Morris JG (1971) Oxygen and the growth and metabolism of Clostridium acetobutylicum. J Gen Microbiol 68(3):307–318.  https://doi.org/10.1099/00221287-68-3-307 CrossRefPubMedGoogle Scholar
  71. Österlund T, Nookaew I, Bordel S, Nielsen J (2013) Mapping condition-dependent regulation of metabolism in yeast through genome-scale modeling. BMC Syst Biol 7(1):36.  https://doi.org/10.1186/1752-0509-7-36 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Paltauf F, Schatz G (1969) Promitochondria of anaerobically grown yeast. II. Lipid composition. Biochemistry 8(1):335–339.  https://doi.org/10.1021/bi00829a046 CrossRefPubMedGoogle Scholar
  73. Payne JL, Boyer AG, Brown JH, Finnegan S, Kowalewski M, Krause RA, Lyons SK, McClain CR, McShea DW, Novack-Gottshall PM, Smith FA, Stempien JA, Wang SC (2009) Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc Natl Acad Sci U S A 106(1):24–27.  https://doi.org/10.1073/pnas.0806314106 CrossRefPubMedGoogle Scholar
  74. Plugge CM (2005) Anoxic media design, preparation, and considerations. Methods Enzymol 397:3–16.  https://doi.org/10.1016/S0076-6879(05)97001-8 CrossRefPubMedGoogle Scholar
  75. Pronk JT, Steensma HY, van Dijken JP (1996) Pyruvate metabolism in Saccharomyces cerevisiae. Yeast 12:1607–1633. doi: 10.1002/(SICI)1097-0061(199612)12:16&lt;1607::AID-YEA70&gt;3.0.CO;2–4Google Scholar
  76. Rodrigues F, Corte-Real M, Leao C, van Dijken JP, Pronk JT (2001) Oxygen requirements of the food spoilage yeast Zygosaccharomyces bailii in synthetic and complex media. Appl Environ Microbiol 67(5):2123–2128.  https://doi.org/10.1128/aem.67.5.2123-2128.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Rohde RA, Price PB (2007) Diffusion-controlled metabolism for long-term survival of single isolated microorganisms trapped within ice crystals. Proc Natl Acad Sci U S A 104(42):16592–16597.  https://doi.org/10.1073/pnas.0708183104 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Rosenfeld E, Beauvoit B (2003) Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae. Yeast 20(13):1115–1144.  https://doi.org/10.1002/yea.1026 CrossRefPubMedGoogle Scholar
  79. Saint-Gobain (2017) Permeability coefficients for peristaltic pump tubings. In: saint-gobain.com. http://www.plasia-tw.saint-gobain.com/uploadedFiles/SGtygon/Documents/Tygon_Tubing/Tygon-PeristalticPumps-Permeability.pdf. Accessed 18 Sep 2017
  80. Salmon J-M, Fornairon-Bonnefond C, Barre P (1998) Determination of oxygen utilization pathways in an industrial strain of Saccharomyces cerevisiae during enological fermentation. J Ferment Bioeng 86(2):154–163.  https://doi.org/10.1016/S0922-338X(98)80054-8 CrossRefGoogle Scholar
  81. Schulze U, Lidén G, Nielsen J, Villadsen J (1996) Physiological effects of nitrogen starvation in an anaerobic batch culture of Saccharomyces cerevisiae. Microbiology 142(8):2299–2310.  https://doi.org/10.1099/13500872-142-8-2299 CrossRefPubMedGoogle Scholar
  82. Scott GR (2011) Elevated performance: the unique physiology of birds that fly at high altitudes. J Exp Biol 214(15):2455–2462.  https://doi.org/10.1242/jeb.052548 CrossRefPubMedGoogle Scholar
  83. Simpson R, Sastry SK (2013) Scale-up in chemical and bioprocess engineering. In: Chemical and bioprocess engineering. Springer New York, New York, NY, pp 261–275.  https://doi.org/10.1007/978-1-4614-9126-2_10 CrossRefGoogle Scholar
  84. Snoek IS, Steensma HY (2006) Why does Kluyveromyces lactis not grow under anaerobic conditions? Comparison of essential anaerobic genes of Saccharomyces cerevisiae with the Kluyveromyces lactis genome. FEMS Yeast Res 6(3):393–403.  https://doi.org/10.1111/j.1567-1364.2005.00007.x CrossRefPubMedGoogle Scholar
  85. Soustre I, Dupuy PH, Silve S, Karst F, Loison G (2000) Sterol metabolism and ERG2 gene regulation in the yeast Saccharomyces cerevisiae. FEBS Lett 470(2):102–106.  https://doi.org/10.1016/S0014-5793(00)01300-4 CrossRefPubMedGoogle Scholar
  86. Speers AM, Cologgi DL, Reguera G (2009) Anaerobic cell culture. Curr Protoc Microbiol 12:A.4F.1–A.4F.16.  https://doi.org/10.1002/9780471729259.mca04fs12 Google Scholar
  87. Stier TJB, Scalf RE, Brockmann MC (1950a) An all-glass apparatus for the continuous cultivation of yeast under anaerobic conditions. J Bacteriol 59(1):45–49PubMedPubMedCentralGoogle Scholar
  88. Stier TJB, Scalf RE, Peter CJ (1950b) Edible oils as sources of lipid anaerobic growth factors for distillers’ yeast. J Cell Compar Physl 36(2):159–163.  https://doi.org/10.1002/jcp.1030360204 CrossRefGoogle Scholar
  89. Storz G, Tartaglia LA, Farr SB, Ames BN (1990) Bacterial defenses against oxidative stress. Trends Genet 6(11):363–368.  https://doi.org/10.1016/0168-9525(90)90278-E CrossRefPubMedGoogle Scholar
  90. Thomas KC, Hynes SH, Ingledew WM (1998) Initiation of anaerobic growth of Saccharomyces cerevisiae by amino acids or nucleic acid bases: ergosterol and unsaturated fatty acids cannot replace oxygen in minimal media. J Ind Microbiol Biotechnol 21(4-5):247–253.  https://doi.org/10.1038/sj.jim.2900584 CrossRefGoogle Scholar
  91. Twigg RS (1945) Oxidation-reduction aspects of resazurin. Nature 155(3935):401–402.  https://doi.org/10.1038/155401a0 CrossRefGoogle Scholar
  92. Tyack PL, Johnson M, Soto NA, Sturlese A, Madsen PT (2006) Extreme diving of beaked whales. J Exp Biol 209(21):4238–4253.  https://doi.org/10.1242/jeb.02505 CrossRefPubMedGoogle Scholar
  93. Valachovic M, Hronská L, Hapala I (2001) Anaerobiosis induces complex changes in sterol esterification pattern in the yeast Saccharomyces cerevisiae. FEMS Microbiol Lett 197(1):41–45.  https://doi.org/10.1111/j.1574-6968.2001.tb10580.x CrossRefPubMedGoogle Scholar
  94. Valero E, Millán C, Ortega JM (2001) Influence of oxygen addition during growth phase on the biosynthesis of lipids in Saccharomyces cerevisiae (M330-9) in enological fermentations. J Biosci Bioeng 92(1):33–38.  https://doi.org/10.1016/S1389-1723(01)80195-X CrossRefPubMedGoogle Scholar
  95. Verduyn C, Postma E, Scheffers WA, van Dijken JP (1992) Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8(7):501–517.  https://doi.org/10.1002/yea.320080703 CrossRefPubMedGoogle Scholar
  96. Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990) Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136(3):395–403.  https://doi.org/10.1099/00221287-136-3-395 CrossRefPubMedGoogle Scholar
  97. Visioli LJ, Enzweiler H, Kuhn RC, Schwaab M, Mazutti MA (2014) Recent advances on biobutanol production. Sustain Chem Process 2(1):15.  https://doi.org/10.1186/2043-7129-2-15 CrossRefGoogle Scholar
  98. Visser W, Scheffers WA, Batenburg-van der Vegte WH, van Dijken JP (1990) Oxygen requirements of yeasts. Appl Environ Microbiol 56(12):3785–3792PubMedPubMedCentralGoogle Scholar
  99. Waldbauer JR, Newman DK, Summons RE (2011) Microaerobic steroid biosynthesis and the molecular fossil record of Archean life. Proc Natl Acad Sci U S A 108(33):13409–13414.  https://doi.org/10.1073/pnas.1104160108 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Wallace PG, Huang M, Linnane AW (1968) The biogenesis of mitochondria. II. The influence of medium composition on the cytology of anaerobically grown Saccharomyces cerevisiae. J Cell Biol 37(2):207–220.  https://doi.org/10.1083/jcb.37.2.207 CrossRefPubMedPubMedCentralGoogle Scholar
  101. Watson K, Rose AH (1980) Fatty-acyl composition of the lipids of Saccharomyces cerevisiae grown aerobically or anaerobically in media containing different fatty acids. Microbiology 117(1):225–233.  https://doi.org/10.1099/00221287-117-1-225 CrossRefGoogle Scholar
  102. Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep-Sea Res Oceanogr Abstr 17(4):721–735.  https://doi.org/10.1016/0011-7471(70)90037-9 CrossRefGoogle Scholar
  103. Wimpenny JW, Necklen DK (1971) The redox environment and microbial physiology. I. The transition from anaerobiosis to aerobiosis in continuous cultures of facultative anaerobes. BBA Bioenergetics 253(2):352–359.  https://doi.org/10.1016/0005-2728(71)90039-9 CrossRefPubMedGoogle Scholar
  104. Yin J, Li G, Ren X, Herrler G (2007) Select what you need: a comparative evaluation of the advantages and limitations of frequently used expression systems for foreign genes. J Biotechnol 127(3):335–347.  https://doi.org/10.1016/j.jbiotec.2006.07.012 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Bruno Labate Vale da Costa
    • 1
    • 2
  • Thiago Olitta Basso
    • 2
  • Vijayendran Raghavendran
    • 1
    • 3
  • Andreas Karoly Gombert
    • 1
  1. 1.School of Food EngineeringUniversity of CampinasCampinasBrazil
  2. 2.Department of Chemical EngineeringUniversity of Sao PauloSão PauloBrazil
  3. 3.Department of Biology and Biological EngineeringChalmers University of TechnologyGöteborgSweden

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