Association of improved oxidative stress tolerance and alleviation of glucose repression with superior xylose-utilization capability by a natural isolate of Saccharomyces cerevisiae

Abstract

BackgroundSaccharomyces cerevisiae wild strains generally have poor xylose-utilization capability, which is a major barrier for efficient bioconversion of lignocellulosic biomass. Laboratory adaption is commonly used to enhance xylose utilization of recombinant S. cerevisiae. Apparently, yeast cells could remodel the metabolic network for xylose metabolism. However, it still remains unclear why natural isolates of S. cerevisiae poorly utilize xylose. Here, we analyzed a unique S. cerevisiae natural isolate YB-2625 which has superior xylose metabolism capability in the presence of mixed-sugar. Comparative transcriptomic analysis was performed using S. cerevisiae YB-2625 grown in a mixture of glucose and xylose, and the model yeast strain S288C served as a control. Global gene transcription was compared at both the early mixed-sugar utilization stage and the latter xylose-utilization stage.ResultsGenes involved in endogenous xylose-assimilation (XYL2 and XKS1), gluconeogenesis, and TCA cycle showed higher transcription levels in S. cerevisiae YB-2625 at the xylose-utilization stage, when compared to the reference strain. On the other hand, transcription factor encoding genes involved in regulation of glucose repression (MIG1, MIG2, and MIG3) as well as HXK2 displayed decreased transcriptional levels in YB-2625, suggesting the alleviation of glucose repression of S. cerevisiae YB-2625. Notably, genes encoding antioxidant enzymes (CTT1, CTA1, SOD2, and PRX1) showed higher transcription levels in S. cerevisiae YB-2625 in the xylose-utilization stage than that of the reference strain. Consistently, catalase activity of YB-2625 was 1.9-fold higher than that of S. cerevisiae S288C during the xylose-utilization stage. As a result, intracellular reactive oxygen species levels of S. cerevisiae YB-2625 were 43.3 and 58.6% lower than that of S288C at both sugar utilization stages. Overexpression of CTT1 and PRX1 in the recombinant strain S. cerevisiae YRH396 deriving from S. cerevisiae YB-2625 increased cell growth when xylose was used as the sole carbon source, leading to 13.5 and 18.1%, respectively, more xylose consumption.ConclusionsEnhanced oxidative stress tolerance and relief of glucose repression are proposed to be two major mechanisms for superior xylose utilization by S. cerevisiae YB-2625. The present study provides insights into the innate regulatory mechanisms underlying xylose utilization in wild-type S. cerevisiae, which benefits the rapid development of robust yeast strains for lignocellulosic biorefineries.Electronic supplementary materialThe online version of this article (10.1186/s13068-018-1018-y) contains supplementary material, which is available to authorized users.

d‐Xylose consumption by nonrecombinant Saccharomyces cerevisiae: A review

“…Clustering of the expression patterns and GO term analysis of each cluster revealed that genes involved in translation, ribosome biogenesis, vesicle‐mediated transport, and cellular localization (among other related processes) were up‐regulated during growth on xylose by the strains having the XDH1 dehydrogenase, confirming that the yeast cells were indeed growing. Other genes up‐regulated during growth on xylose were enriched for pentose metabolic process, and response to oxidative stress, as also shown latter on by Cheng and co‐workers (). Some set of genes induced by xylose consumption or growth on xylose have been also observed to be up‐regulated during xylulose fermentation (see above, Mittelman & Barkai, ; Tamari et al, ).…”

“…Under these conditions strain YB2625 produced 10.9 g/L xylitol, and strain S288C produced 3.1 g/L, without significant differences in the ethanol concentration in the fermentation media. However, significant differences in the production of glycerol and acetic acid were observed (higher with S288C), as well as a slightly higher biomass produced by strain YB2625 throughout the culture (Cheng et al, ).…”

“…In order to better understand the natural capacity of some S. cerevisiae strains to consume/grow on xylose, two publications have reported comparative transcriptomic analysis of nonrecombinant yeast strains during xylose consumption (Cheng et al, ; Wenger et al, ). Cheng and co‐workers () used the nonrecombinant strain YB‐2625 under conditions of glucose/xylose co‐fermentation and compared this strain with the laboratory S288C strain in two conditions: xylose utilization phase by both strains (first 7 hr of fermentation), and after 48 hr when only strain YB‐2625 continued to consume xylose. Their RNA‐seq results showed that 1.637 genes were differentially expressed (1.313 down‐regulated and 324 up‐regulated) in the nonrecombinant yeast strain at 7 hr of fermentation, and 2.004 genes (1.727 down‐regulated and 277 up‐regulated) were differentially expressed in strain YB‐2625 during the xylose utilization stage.…”

“…All these expression profiles indicate that endogenous XDH is a bottleneck for natural yeast to metabolize xylose. The available data also suggests that strain YB‐2625 shows a lower glucose repression, increased expression of oxidative stress‐responsive genes, as well as of genes involved in gluconeogenesis, TCA cycle, and ergosterol biosynthesis (Cheng et al, ).…”

“…Based on the transcriptome data of the natural strain YB‐2625 capable of consuming xylose, which showed increased expression of oxidative stress‐responsive genes, Cheng and co‐workers () were able to improve by 13–18% xylose consumption by a recombinant yeast strain (isogenic to YB‐2625) overexpressing the cytosolic catalase encoded by CTT1 or the mitochondrial peroxidase encoded by PRX1 . Unfortunately, these authors did not test if such overexpressions would increase xylose consumption by the native strain YB‐2625.…”