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Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model.
Front Microbiol 2018; 9:291FM

Abstract

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.

Authors+Show Affiliations

Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.Mathomics, Center for Mathematical Modeling, Universidad de Chile, Santiago, Chile. Center for Genome Regulation, Universidad de Chile, Santiago, Chile.Department of Chemical and Bioprocess Engineering, School of Engineering, Pontificia Universidad Católica de Chile, Santiago, Chile.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

29545779

Citation

Contreras, Angela, et al. "Mapping the Physiological Response of Oenococcus Oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model." Frontiers in Microbiology, vol. 9, 2018, p. 291.
Contreras A, Ribbeck M, Gutiérrez GD, et al. Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model. Front Microbiol. 2018;9:291.
Contreras, A., Ribbeck, M., Gutiérrez, G. D., Cañon, P. M., Mendoza, S. N., & Agosin, E. (2018). Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model. Frontiers in Microbiology, 9, p. 291. doi:10.3389/fmicb.2018.00291.
Contreras A, et al. Mapping the Physiological Response of Oenococcus Oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model. Front Microbiol. 2018;9:291. PubMed PMID: 29545779.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Mapping the Physiological Response of Oenococcus oeni to Ethanol Stress Using an Extended Genome-Scale Metabolic Model. AU - Contreras,Angela, AU - Ribbeck,Magdalena, AU - Gutiérrez,Guillermo D, AU - Cañon,Pablo M, AU - Mendoza,Sebastián N, AU - Agosin,Eduardo, Y1 - 2018/03/01/ PY - 2017/10/22/received PY - 2018/02/07/accepted PY - 2018/3/17/entrez PY - 2018/3/17/pubmed PY - 2018/3/17/medline KW - Oenococcus oeni KW - genome-scale metabolic model KW - lactic acid bacteria KW - malolactic fermentation KW - physiological ethanol response KW - wine-like defined culture medium SP - 291 EP - 291 JF - Frontiers in microbiology JO - Front Microbiol VL - 9 N2 - 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. SN - 1664-302X UR - https://www.unboundmedicine.com/medline/citation/29545779/Mapping_the_Physiological_Response_of_Oenococcus_oeni_to_Ethanol_Stress_Using_an_Extended_Genome_Scale_Metabolic_Model_ L2 - https://dx.doi.org/10.3389/fmicb.2018.00291 DB - PRIME DP - Unbound Medicine ER -