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

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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.

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Change history

  • 27 April 2018

    The published online version contains mistake in Figure1. In the x-axis, instead of “1000”, the number should be “100”.

Notes

  1. 1.

    A cylindrical reactor with height (h) and radius (r) has a lateral surface area of 2πrh and a volume of πr2h. The surface area to volume is inversely proportional to the radius of the reactor; thus, the larger the reactor, the smaller the surface area to volume. This has profound consequences for heat and mass transfer. Heat transfer is proportional to the surface area, whilst the metabolic heat generation is proportional to the culture volume. Thus, at very large volumes (and large radii), the available heat transfer area is insufficient to dissipate the heat that is generated. Unlike laboratory reactors which are well mixed, there will be concentration gradients in large-scale reactors affecting the mass transfer of O2, as well as other nutrients, vastly affecting the cellular physiology.

  2. 2.

    \( \mathrm{Partial}\kern0.34em \mathrm{pressure}\mathrm{of}{\mathrm{O}}_2=\mathsf{T}\mathrm{otal}\kern0.34em \mathrm{pressure}\times \mathrm{mole}\kern0.34em \mathrm{fraction} \) of O2 in the gas

  3. 3.

    Barrer is a non-SI unit for gas permeability. \( 1\ \mathrm{barrer}={10}^{-10}\times \frac{{\mathrm{cm}}^3\times \mathrm{cm}}{{\mathrm{cm}}^2\times \mathrm{s}\times \mathrm{cm}\ \mathrm{Hg}} \)

  4. 4.

    For a tubing of 30-cm length, having an internal diameter of 0.31 cm, the diffusion rate of O2 can be calculated using this relation, for a partial pressure of O2 of 15.6 cm Hg and molar volume of 22,400 cm3: \( {\mathrm{O}}_2\kern0.2em \mathrm{diffusion}\kern0.34em \mathrm{rate}\kern0.2em \left(\frac{\upmu \mathrm{mol}}{\mathrm{h}}\right)=\frac{\mathrm{surfaceareacm}2\mathrm{xpermeabilityxPO}2\mathrm{cmHg}}{\mathrm{thicknesscm}}. \) The rate of O2 diffusing through a norprene tubing is 1.5 μmol h−1, whilst it is 59 μmol h−1 with a silicone tubing.

  5. 5.

    Oleate requires 1 mol of O2, and ergosterol requires 12 mol of O2 to be synthesized. For an ergosterol and an oleate content of 0.2 and 3.5% per dry cell mass, the amount of O2 needed for their biosynthesis is 185 μmol gDCM−1, assuming the consumed O2 is used only for these two reactions. For a biomass yield of 0.1 g gglucose−1, a dilution rate of 0.1 h−1 and a glucose concentration in the feeding medium of 10 g L−1, steady-state biomass would be 1 gDCM L−1. Thus, the O2 demand is \( 185\left(\frac{\upmu \mathrm{mol}\ {\mathrm{O}}_2\ \mathrm{needed}}{{\mathrm{g}}_{\mathrm{DCM}}\ \mathrm{produced}}\right)\times 0.10\frac{\left(\frac{{\mathrm{g}}_{\mathrm{DCM}}\ \mathrm{produced}}{{\mathrm{g}}_{\mathrm{DCM}}\ \mathrm{present}}\right)}{\mathrm{h}}\times 1\ {\mathrm{g}}_{\mathrm{DCM}}=18.5\frac{\upmu \mathrm{mol}\ {\mathrm{O}}_2}{\mathrm{h}} \)

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Funding

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.

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Correspondence to Andreas Karoly Gombert.

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da Costa, B.L.V., Basso, T.O., Raghavendran, V. et al. Anaerobiosis revisited: growth of Saccharomyces cerevisiae under extremely low oxygen availability. Appl Microbiol Biotechnol 102, 2101–2116 (2018). https://doi.org/10.1007/s00253-017-8732-4

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Keywords

  • Anaerobiosis
  • Oxygen
  • Saccharomyces cerevisiae
  • Chemostat cultivation
  • Anaerobic growth factors