The response mechanism of bacteria to ethanol stress in malolactic fermentation
GE Yuzi1, SUN Jingxian1, HUANG Gang1, JIN Gang2,3,4*
1(School of Agriculture, Ningxia University, Yinchuan 750021, China) 2(School of Food and Wine, Ningxia University, Yinchuan 750021, China) 3(Engineering Research Center of Ministry of Grape and Wine, Yinchuan 750021, China) 4(Ningxia Grape and Wine Engineering Technology Center, Yinchuan 750021, China)
Abstract: Malolactic fermentation (MLF) caused by lactic acid bacteria (LAB) is a necessary process in high-quality wine production. In this process, ethanol is the main factor that inhibit the activity of LAB. With the increase of sugar content in grapes caused by global warming, focus has been placed on the inhibitory effect of ethanol on LAB. Ethanol stress changes the cell structure of LAB and affects the MLF. Therefore, the growth and metabolism of LAB under ethanol stress are very important for wine production. The response mechanism of common LAB under ethanol stress during MLF is described, which provides a reference for the ethanol stress tolerance mechanism of LAB, as well as the screening of strains.
盖昱梓,孙静娴,黄刚,等. 苹果酸-乳酸发酵细菌乙醇胁迫应答机制研究进展[J]. 食品与发酵工业, 2021, 47(3): 288-293.
GE Yuzi,SUN Jingxian,HUANG Gang,et al. The response mechanism of bacteria to ethanol stress in malolactic fermentation[J]. Food and Fermentation Industries, 2021, 47(3): 288-293.
[1] BRIZUELA S N,BRAVO-FERRADA M B,POZO-BAYÓN Á M,et al.Changes in the volatile profile of pinot noir wines caused by patagonian Lactobacillus plantarum and Oenococcus oeni strains[J].Food Research International,2018,106:22-28. [2] BRIZUELA S N,BRAVO-FERRADA M B,HENS V L D,et al.Comparative vinification assays with selected patagonian strains of Oenococcus oeni and Lactobacillus plantarum[J].LWT-Food Science and Technology,2016,77:348-355. [3] CAPPELLO M S,ZAPPAROLI G,LOGRIECO A,et al.Linking wine lactic acid bacteria diversity with wine aroma and flavor[J].International Journal of Food Microbiology,2017,243:16-27. [4] UBEDA C,HORNEDO-ORTEGA R,CEREZO B A,et al.Chemical hazards in grapes and wine,climate change and challenges to face[J].Food Chemistry,2020,314.DOI:100.1016/j.foodchem.2020.126222. [5] 金刚. 苹果酸-乳酸发酵细菌的多样性及其耐酒精分析[D].杨凌:西北农林科技大学,2015. JIN G.Study on diversity and ethanol tolerance of malolactic bacteria[D].Ynagling:Northwest A&F University,2015. [6] ZHANG Y M,ROCK C O.Membrane lipid homeostasis in bacteria[J].Nature Reviews Microbiology,2008,6(3):222-233. [7] 王婷婷, 李春,李佳栋,等.乙醇胁迫对植物乳杆菌膜生理及黏附性的影响[J].食品科学,2019,40(18):63-69. Wang T T,LI C,LI J D,et al.Effect of ethanol stress on membrane physiology and adhesion of Lactobacillus plantarum[J].Food Science,2019,40(18):63-69. [8] LAN C H,MARECHAL P A,MAI L T,et al.Fluorescent probes to evaluate the physiological state and activity of microbial biocatalysts:A guide for prokaryotic and eukaryotic investigation[J].Biotechnology Journal,2008,3(7):890-903. [9] VAN B D V H,ABEE T,TEMPELAARS M,et al.Short-and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum[J].Applied and Environmental Microbiology,2011,77(15):5 247-5 256. [10] BRAVO-FERRADA M B,GÓMEZ-ZAVAGLIA A,SEMORILE L,et al.Effect of the fatty acid composition of acclimated oenological Lactobacillus plantarumon the resistance to ethanol[J].Letters in Applied Microbiology,2014,60(2):155-161. [11] YANG X,TENG K,LI L,et al.Transcriptional regulator AcrR increases ethanol tolerance through regulating fatty acid synthesis in Lactobacillus plantarum[J].Applied and Environmental Microbiology,2019,85(22).DOI:10.1128/aem.01690-19. [12] 赵红玉, 李华,刘龙祥,等.酒酒球菌胁迫适应性机制的研究进展[J].中国食品学报,2019,48(4):556-561. ZHAO H Y,LI H,LIU L X.The research progress of stress adaptation mechanism of Oenococcus oeni[J].Journal of Chinese Institute of Food Science and Technology,2019,48(4):556-561. [13] 李中超. 酒酒球菌SD-2a质膜H+-ATPase特性的研究[D].杨凌:西北农林科技大学,2009. LI Z C.Researches on the characteristics of plasma membrane H+-ATPase of Oenococcus oeni SD-2a[D].Yangling:Northwest A&F University,2009. [14] CAFARO C,BONOMO M G,SALZANO G.Adaptive changes in geranylgeranyl pyrophosphate synthase gene expression level under ethanol stress conditions in Oenococcus oeni[J].Journal of Applied Microbiology,2013,116(1):71-80. [15] NICOLAOU S A,GAIDA S M,PAPOUTSAKIS E T.Exploring the combinatorial genomic space in Escherichia coli for ethanol tolerance[J].Biotechnology Journal,2012,7(11):1 337-1 345. [16] VOLLMER W,BLANOT D,DE PEDRO M A.Peptidoglycan structure and architecture[J].Fems Microbiology Reviews,2008,32(2):149-167. [17] YUAN Y,BI C,NICOLAOU S A,et al.Overexpression of the Lactobacillus plantarum peptidoglycan biosynthesis murA2 gene increases the tolerance of Escherichia coli to alcohols and enhances ethanol production[J].Applied Microbiology and Biotechnology,2014,98(19):8 399-8 411. [18] OLGUÍN N,CHAMPOMIER-VERGES M,ANGLADE P,et al.Transcriptomic and proteomic analysis of Oenococcus oeni PSU-1 response to ethanol shock[J].Food Microbiology,2015,51:87-95. [19] DIMOPOULOU M,HAZO L,DOLS-LAFARGUE M.Exploration of phenomena contributing to the diversity of Oenococcus oeni exopolysaccharides[J].International Journal of Food Microbiology,2012,153(1-2):114-122. [20] CIEZACK G,HAZO L,CHAMBAT G,et al.Evidence for exopolysaccharide production by Oenococcus oeni strains isolated from non-ropy wines[J].Journal of Applied Microbiology,2010,108(2):499-509. [21] COSTANTINI A,RANTSIOU K,MAJUMDER A,et al.Complementing DIGE proteomics and DNA subarray analyses to shed light on Oenococcus oeni adaptation to ethanol in wine-simulated conditions[J].Journal of Proteomics,2015,123:114-127. [22] SALEMA M,LOLKEMA J S,SAN ROMÃO M V,et al.The proton motive force generated in Leuconostoc oenos by L-malate fermentation[J].Journal of Bacteriology,1996,178(11):3 127-3 132. [23] GAO Y,LIU Y,SUN M,et al.Physiological function analysis of Lactobacillus plantarum Y44 based on genotypic and phenotypic characteristics[J].Journal of Dairy Science,2020,103:5 916-5 939. [24] MARGALEF-CATALA M,FELIS G E,REGUANT C,et al.Identification of variable genomic regions related to stress response in Oenococcus oeni[J].Food Research International,2017,102:625-638. [25] CONTRERAS A,RIBBECK M,GUTIÉRREZ G D,et al.Mapping the physiological response of Oenococcus oeni to ethanol stress using an extended genome-scale metabolic model[J].Frontiers in Microbiology,2018,9:291. [26] ZHANG J,DU G C,ZHANG Y,et al.Glutathione protects Lactobacillus sanfranciscensis against freeze-thawing,freeze-drying,and cold treatment[J].Applied and Environmental Microbiology,2010,76(9):2 989-2 996. [27] SAMAD A,JAMES A,WONG J,et al.Insulin protects pancreatic acinar cells from palmitoleic acid-induced cellular injury[J].Journal of Biological Chemistry,2014,289:23 582-23 595. [28] CHU-KY S,TOURDOT-MARECHAL R,MARECHAL P-A,et al.Combined cold,acid,ethanol shocks in Oenococcus oeni:Effects on membrane fluidity and cell viability[J].Biochimica Et Biophysica Acta,2005,1717(2):118-124. [29] LIN Y,ZHAO H Y,LIU L X,et al.Heterologous expression of the puuE from Oenococcus oeni SD-2a in Lactobacillus plantarum WCFS1 improves ethanol tolerance[J].Journal of Basic Microbiology,2019,59(11):1-9. [30] MOHEDANO M D I L,RUSSO P,DE L R V,et al.A proteome reference map of the wine lactic acid bacteria Oenococcus oeni ATCC BAA-1163[J].Open Biology,2014,4(2):130-154. [31] ZHAO W Y,KANG Z K.Advanced progress on adaptive stress response of Oenococcus oeni[J].Journal of Northeast Agricultural University,2013,20(1),91-96. [32] PASSERINI D,LAROUTE,VALÉRIE,et al.New insights into Lactococcus lactis diacetyl-and acetoin-producing strains isolated from diverse origins[J].International Journal of Food Microbiology,2013,160(3):329-336. [33] OLGUIN N,BORDONS A,REGUANT C.Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni[J].Food microbiology,2009,26(2):197-203. [34] ZOMER A L,BUIST G,LARSEN R,et al.Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp.cremoris MG1363[J].Journal of Bacteriology,2006,189(4),1 366-1 381. [35] DÍEZ L,SOLOPOVA A,FERNÁNDEZ-PÉREZ R,et al.Transcriptome analysis shows activation of the arginine deiminase pathway in Lactococcus lactis as a response to ethanol stress[J].International Journal of Food Microbiology,2017,257:41-48. [36] HEBERT E M,RAYA R R,DE GIORI G S.Nutritional requirements and nitrogen-dependent regulation of proteinase activity of Lactobacillus helveticus CRL 1062[J].Applied and Environmental Microbiology,2000,66(12):5 316-5 321. [37] PAPADIMITRIOU K,ALEGRIA A,BRON P A,et al.Stress physiology of lactic acid bacteria[J].Microbiology and Molecular Biology Reviews,2016,80:837-890. [38] ZOTTA T,PARENTE E,RICCIARDI A.Aerobic metabolism in the genus Lactobacillus:Impact on stress response and potential applications in the food industry[J].Journal of Applied Microbiology,2017,122:857-869. [39] MAZZOLI R,PESSIONE E,DUFOUR M,et al.Glutamate induced metabolic changes in Lactococcus lactis NCDO 2118 during GABA production:Combined transcriptomic and proteomic analysis[J].Amino Acids,2010,39(3):727-737. [40] MASIP L,VEERAVALLI K,GEORGIOU G.The many faces of glutathione in bacteria[J].Antioxidants & Redox Signaling,2006,8(5-6):753-762. [41] CECCONI D,MILLI A,RINALDUCCI S,et al.Proteomic analysis of Oenococcus oeni freeze-dried culture to assess the importance of cell acclimation to conduct malolactic fermentation in wine[J].Electrophoresis,2009,30(17):2 988-2 995. [42] MARGALEF-CATALÀ M,ARAQUE I,BORDONS A,et al.Genetic and transcriptional study of glutathione metabolism in Oenococcus oeni[J].International Journal of Food Microbiology,2017,242:61-69. [43] MARGALEF-CATALÀ M,ARAQUE I,WEIDMANN S,et al.Protective role of glutathione addition against wine-related stress in Oenococcus oeni[J].Food Research International,2016,90:8-15. [44] CEBRIÁN G,CONDÓN S,MAÑAS P.Heat resistance,membrane fluidity and sublethal damage in Staphylococcus aureus cells grown at different temperatures[J].International Journal of Food Microbiology,2019,289:49-56. [45] VALERIANO V D,PARUNGAO-BALOLONG M,Kang D K.In vitro evaluation of the mucin-adhesion ability and probiotic of Lactobacillus mucosae LM1[J].Journal of pplied Microbiology,2014,117:485-497. [46] GRANDVALET C,COUCHENEY F,BELTRAMO C,et al.CTSR is the master regulator of stress response gene expression in Oenococcus oeni[J].Journal of Bacteriology,2005,187:5 614-5 623. [47] DARSONVAL M,JULLIAT F,MSADEK T,et al.CTSR,the master regulator of stress-response in Oenococcus oeni,is a heat sensor interacting with ClpL1[J].Frontiers in Microbiology,2018,9:3 135. [48] ZHAO H,YUAN L,HU K,et al.Heterologous expression of ctsR from Oenococcus oeni enhances the acid-ethanol resistance of Lactobacillus plantarum[J].FEMS Microbiology Letters,2019,366(15).DOI:10.1093/femsle/fnz192. [49] FREES D,SAVIJOKI K,VARMANEN P,et al.Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC,Gram-positive bacteria[J].Molecular Microbiology,2010,63(5):1 285-1 295. [50] 王艳霞. 简单节杆菌乙醇胁迫条件下的抗逆机制研究[D].天津:天津科技大学,2015. WANG Y X.Study on tolerance mechanism of Arthtrobacter simplex under ethanol stress[D].Tianjin:Tianjin University of Science and Technology,2015.
2021, Vol. 47 
