Changes in lipid metabolism convey acid tolerance in Saccharomyces cerevisiae

Zhong-Peng Guo,Jens Nielsen,Sakda Khoomrung,Lisbeth Olsson

doi:10.1186/s13068-018-1295-5

Abstract

BackgroundThe yeast Saccharomyces cerevisiae plays an essential role in the fermentation of lignocellulosic hydrolysates. Weak organic acids in lignocellulosic hydrolysate can hamper the use of this renewable resource for fuel and chemical production. Plasma-membrane remodeling has recently been found to be involved in acquiring tolerance to organic acids, but the mechanisms responsible remain largely unknown. Therefore, it is essential to understand the underlying mechanisms of acid tolerance of S. cerevisiae for developing robust industrial strains.ResultsWe have performed a comparative analysis of lipids and fatty acids in S. cerevisiae grown in the presence of four different weak acids. The general response of the yeast to acid stress was found to be the accumulation of triacylglycerols and the degradation of steryl esters. In addition, a decrease in phosphatidic acid, phosphatidylcholine, phosphatidylserine and phosphatidylethanolamine, and an increase in phosphatidylinositol were observed. Loss of cardiolipin in the mitochondria membrane may be responsible for the dysfunction of mitochondria and the dramatic decrease in the rate of respiration of S. cerevisiae under acid stress. Interestingly, the accumulation of ergosterol was found to be a protective mechanism of yeast exposed to organic acids, and the ERG1 gene in ergosterol biosynthesis played a key in ergosterol-mediated acid tolerance, as perturbing the expression of this gene caused rapid loss of viability. Interestingly, overexpressing OLE1 resulted in the increased levels of oleic acid (18:1n-9) and an increase in the unsaturation index of fatty acids in the plasma membrane, resulting in higher tolerance to acetic, formic and levulinic acid, while this change was found to be detrimental to cells exposed to lipophilic cinnamic acid.ConclusionsComparison of lipid profiles revealed different remodeling of lipids, FAs and the unsaturation index of the FAs in the cell membrane in response of S. cerevisiae to acetic, formic, levulinic and cinnamic acid, depending on the properties of the acid. In future work, it will be necessary to combine lipidome and transcriptome analysis to gain a better understanding of the underlying regulation network and interactions between central carbon metabolism (e.g., glycolysis, TCA cycle) and lipid biosynthesis.

Highlights

Weak organic acids such as acetic, formic and levulinic acids are present in lignocellulosic hydrolysate as potential inhibitors that can hamper the use of this renewable resource for fuel and chemical production [1]
Physiological response of S. cerevisiae to weak acids Under the reference condition, yeast started to grow on glucose without a lag phase, at μmax reaching 0.41 h−1 followed by a second growth phase on the ethanol produced during the glucose growth phase (Table 1)
It was noted that 0.17 mM undissociated cinnamic acid, a much smaller amount than the other acids, led to a 50% reduction in the biomass yield (Table 1), which indicates that the hydrophobicity of the acid governs the toxicity of the acid

Summary

Introduction

Weak organic acids such as acetic, formic and levulinic acids are present in lignocellulosic hydrolysate as potential inhibitors that can hamper the use of this renewable resource for fuel and chemical production [1]. The yeast Saccharomyces cerevisiae plays an essential role in the fermentation of lignocellulosic hydrolysates. Acetic acid in particular inhibits NADH dehydrogenase and induces programmed cell death [5, 6] Lipophilic weak acids, such as sorbate and benzoate which are. Responses to weak acids, such as ATP-dependent efflux of the protons and anions, via plasma membrane H +-ATPase Pma1p and the ATP-binding cassette transporter (Pdr12p), have been suggested [11, 12]. Weak organic acids in lignocellulosic hydrolysate can hamper the use of this renewable resource for fuel and chemical production. It is essential to understand the underlying mechanisms of acid tolerance of S. cerevisiae for developing robust industrial strains

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