Genetic and transcriptional study of glutathione metabolism in Oenococcus oeni

Margalef-Català, Mar; Araque, Isabel; Bordons, Albert; Reguant, Cristina

doi:10.1016/j.ijfoodmicro.2016.11.013

Cited by 18 publications

(10 citation statements)

References 42 publications

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“…Other authors have cultured O. oeni PSU-1 in the presence of 12% of ethanol, showing that genes related with malate and citrate consumption were up-regulated while genes related with fructose consumption were down-regulated, which was associated to mechanisms of ethanol resistance ( Margalef-Catalá et al, 2016 ). We observed that malate and citrate were almost totally consumed during the first 48 h of culture (phase I), suggesting that both substrates were critical for O. oeni survival; although we did not find a clear relation between ethanol content and citrate consumption, we did observe an increment in fluxes related with citrate consumption.…”

Section: Discussionmentioning

confidence: 99%

“…Since the genome sequence of O. oeni PSU-1 was released by Mills et al (2005) , several -omic studies have significantly contributed to the understanding of the metabolic changes that occur in this microorganism during the MLF ( Olguín et al, 2009 , 2015 ; Olguin, 2010 ; Bordas et al, 2015 ; Costantini et al, 2015 ; Margalef-Catalá et al, 2016 ; Bartowsky, 2017 ; Sternes et al, 2017 ). Bridier et al (2010) constructed a phylogenetic tree comparing the sequences of the seven housekeeping genes presents in 258 O. oeni strains.…”

Section: Introductionmentioning

confidence: 99%

“… Olguín et al (2015) performed transcriptomic and proteomic analyses which revealed that main genes affected by ethanol (12%v/v) were related with metabolite transport, as well as cell wall and membrane biogenesis; furthermore, they observed relocation of cytosolic proteins in the membrane, as a protective mechanism. More recently, Margalef-Catalá et al (2016) also performed transcriptomic and proteomic analyses, showing that the amino acid metabolism and transport were altered and that several peptidases were up regulated both at gene and protein levels. More recently, Margalef-Catalá et al (2016) also performed transcriptomic and proteomic analyses, showing that the amino acid metabolism and transport mechanisms were altered and that several peptidases were up-regulated both at gene and protein levels.…”

Section: Introductionmentioning

confidence: 99%

“…More recently, Margalef-Catalá et al (2016) also performed transcriptomic and proteomic analyses, showing that the amino acid metabolism and transport were altered and that several peptidases were up regulated both at gene and protein levels. More recently, Margalef-Catalá et al (2016) also performed transcriptomic and proteomic analyses, showing that the amino acid metabolism and transport mechanisms were altered and that several peptidases were up-regulated both at gene and protein levels. Moreover, the authors observed that genes related with malate and citrate uptake were up-regulated, while genes related with fructose consumption were down-regulated.…”

Section: Introductionmentioning

confidence: 99%

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Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model

et al. 2018

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The effect of ethanol on the metabolism of Oenococcus oeni, the bacterium responsible for the malolactic fermentation (MLF) of wine, is still scarcely understood. Here, we characterized the global metabolic response in O. oeni PSU-1 to increasing ethanol contents, ranging from 0 to 12% (v/v). We first optimized a wine-like, defined culture medium, MaxOeno, to allow sufficient bacterial growth to be able to quantitate different metabolites in batch cultures of O. oeni. Then, taking advantage of the recently reconstructed genome-scale metabolic model iSM454 for O. oeni PSU-1 and the resulting experimental data, we determined the redistribution of intracellular metabolic fluxes, under the different ethanol conditions. Four growth phases were clearly identified during the batch cultivation of O. oeni PSU-1 strain, according to the temporal consumption of malic and citric acids, sugar and amino acids uptake, and biosynthesis rates of metabolic products – biomass, erythritol, mannitol and acetic acid, among others. We showed that, under increasing ethanol conditions, O. oeni favors anabolic reactions related with cell maintenance, as the requirements of NAD(P)+ and ATP increased with ethanol content. Specifically, cultures containing 9 and 12% ethanol required 10 and 17 times more NGAM (non-growth associated maintenance ATP) during phase I, respectively, than cultures without ethanol. MLF and citric acid consumption are vital at high ethanol concentrations, as they are the main source for proton extrusion, allowing higher ATP production by F0F1-ATPase, the main route of ATP synthesis under these conditions. Mannitol and erythritol synthesis are the main sources of NAD(P)+, countervailing for 51–57% of its usage, as predicted by the model. Finally, cysteine shows the fastest specific consumption rate among the amino acids, confirming its key role for bacterial survival under ethanol stress. As a whole, this study provides a global insight into how ethanol content exerts a differential physiological response in O. oeni PSU-1 strain. It will help to design better strategies of nutrient addition to achieve a successful MLF of wine.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model

et al. 2018

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“…In the role of reduced glutathione in maintaining sulfur bridges, glutaredoxin reacts with oxidised sulfur bridges where after reduced glutathione recycles glutaredoxin (Masip et al 2006). Interestingly, O. oeni does not have the genes to synthesise glutathione (Pophaly et al 2012), but does have the genes for its turnover and import (Margalef-Català et al 2016b, 2017c. With the concurrent implications of glutathione reductase in the ethanol stress response, a major development in understanding the stress response of O. oeni was recently made when the role of glutathione was clearly demonstrated (Margalef-Català et al 2016b) and its metabolism characterised (Margalef-Català et al 2017a).…”

Section: Role Of Glutathionementioning

confidence: 99%

Oenococcus oeni, a species born and moulded in wine: a critical review of the stress impacts of wine and the physiological responses

Bech‐Terkilsen

Westman

Swiegers

et al. 2020

Australian Journal of Grape and Wine Research

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Oenococcus oeni is a lactic acid bacterium highly adapted to the stressful environment of wine, and is widely used as an industrial starter culture to conduct malolactic fermentation (MLF), the conversion of L-malate to L-lactate. Some cold-climate wine regions still produce wines which prove too stressful for the application of a starter culture, resulting in sluggish or stuck MLFs which compromise the quality and stability of the wine. The literature on the three primary stress factors, low pH, ethanol and SO 2 , is reviewed as well as their toxic mechanisms; possible interactions between the stress factors are also discussed. In particular, the toxic mechanisms of SO 2 , an extremely inhibitory compound, are poorly understood. in vitro studies as well as in vivo studies in other prokaryotes point to numerous mechanisms which could have widespread impacts on the cell envelope, proteins and DNA in O. oeni. We also review the responses of O. oeni to these stress factors and offer a simplified model of events which cultures inoculated into particularly stressful wines may experience. Although significant advances have been made in our understanding of the stress responses in recent years, many fundamental aspects still require study.

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Influences of acid and ethanol stresses on Oenococcus oeniSD‐2a and its proteomic and transcriptional responses

et al. 2020

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BACKGROUND During winemaking, malolactic fermentation (MLF) is usually induced by Oenococcus oeni owing to its high resistance to wine stress factors. To ensure a controlled and efficient MLF process, starter cultures are inoculated in wine. In previous studies, O. oeni strains with sub‐lethal acid or ethanol stresses showed higher freeze‐drying vitality and better MLF performance. To explore the mechanisms involved, influences of acid and ethanol stresses on O. oeni SD‐2a were investigated in this study to gain a better understanding of the cross‐protection responses. RESULTS The results showed that acid and ethanol stresses both caused damage to cell membranes and decreased cellular adenosine triphosphate concentration. At the same time, acid stress increased the uptake of glutathione, while ethanol stress led to cell depolarization. The results of comparative proteomic analysis highlighted that heat shock protein was induced with almost all acid and ethanol stresses. In addition, the expression of stress‐relevant genes (hsp20, clpP, trxA, ctsR, recO, usp) increased greatly with ethanol and acid stress treatments. Finally, the viability of O. oeni was improved with acid and ethanol pretreatments after freeze‐drying. CONCLUSIONS This study demonstrated that acid and ethanol stresses had mixed influences on O. oeni SD‐2a. Some physiological and molecular changes would contribute to a more stress‐tolerant state of O. oeni, thereby improving the viability of lyophilized cells. © 2020 Society of Chemical Industry

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Genetic and transcriptional study of glutathione metabolism in Oenococcus oeni

Cited by 18 publications

References 42 publications

Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model

Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model

Oenococcus oeni, a species born and moulded in wine: a critical review of the stress impacts of wine and the physiological responses

Influences of acid and ethanol stresses on Oenococcus oeniSD‐2a and its proteomic and transcriptional responses

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