Methionine addition improves the acid tolerance of Lactiplantibacillus plantarum by altering cellular metabolic flux, energy distribution, lipids composition

Qiang Meng, Yueyao Li, Yuxin Yuan, Shaowen Wu, Kan Shi, Shuwen Liu

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 48. DOI: 10.1007/s44154-022-00072-z

Methionine addition improves the acid tolerance of Lactiplantibacillus plantarum by altering cellular metabolic flux, energy distribution, lipids composition

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Abstract

This paper reported a wine-derived lactic acid bacterium, Lactiplantibacillus plantarum XJ25, which exhibited higher cell viability under acid stress upon methionine supplementation. Cellular morphology and the composition of the cytomembrane phospholipids revealed a more solid membrane architecture presented in the acid-stressed cells treated with methionine supplementation. Transcriptional analysis showed L. plantarum XJ25 reduced methionine transport and homocysteine biosynthesis under acid stress. Subsequent overexpression assays proved that methionine supplementation could alleviate the cell toxicity from homocysteine accumulation under acid stress. Finally, L. plantarum XJ25 employed energy allocation strategy to response environmental changes by balancing the uptake methionine and adjusting saturated fatty acids (SFAs) in membrane. These data support a novel mechanism of acid resistance involving methionine utilization and cellular energy distribution in LAB and provide crucial theoretical clues for the mechanisms of acid resistance in other bacteria.

Keywords

Acid stress / Lactiplantibacillus plantarum / Methionine / Cell viability / Transcription level / Membrane lipids

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Qiang Meng, Yueyao Li, Yuxin Yuan, Shaowen Wu, Kan Shi, Shuwen Liu. Methionine addition improves the acid tolerance of Lactiplantibacillus plantarum by altering cellular metabolic flux, energy distribution, lipids composition. Stress Biology, 2022, 2(1): 48 https://doi.org/10.1007/s44154-022-00072-z

References

[1]
Brizuela NS, Arnez-Arancibia M, Semorile L, Bravo-Ferrada BM, Tymczyszyn EE (2021) Whey permeate as a substrate for the production of freeze-dried Lactiplantibacillus plantarum to be used as a malolactic starter culture. World J Microbiol Biotechnol 37(7). https://doi.org/10.1007/10.1007/s11274-021-03088-1
[2]
BrizuelaNS, Bravo-FerradaBM, Pozo-BayonMA, Pozo-BayonMA, TymczyszynEE. Changes in the volatile profile of Pinot noir wines caused by Patagonian Lactobacillus plantarum and Oenococcus oeni strains. Food Res Int, 2018, 10: 622-628
CrossRef Google scholar
[3]
BroadbentJR, LarsenRL, DeibelV, SteeleJL. Physiological and transcriptional response of Lactobacillus casei ATCC 334 to acid stress. J Bacteriol, 2010, 192(9):2445-2458
CrossRef Google scholar
[4]
Dato L, Berterame NM, Ricci MA, Paganoni P, Palmieri L, Porro D, Branduardi P (2014) Changes in SAM2 expression affect lactic acid tolerance and lactic acid production in Saccharomyces cerevisiae. Microb Cell Fact 13. https://doi.org/10.1007/10.1186/s12934-014-0147-7
[5]
DengN, DuH, XuY. Cooperative response of Pichia kudriavzevii and Saccharomyces cerevisiae to lactic acid stress in Baijiu fermentation. J Agric Food Chem, 2020, 68(17):4903-4911
CrossRef Google scholar
[6]
FonsecaHC, MeloDS, RamosCL, MenezesAGT, DiasDR, SchwanRF. Sensory and flavor-aroma profiles of passion fruit juice fermented by potentially probiotic Lactiplantibacillus plantarum CCMA 0743 strain. Food Res Int, 2022, 152: 110710
CrossRef Google scholar
[7]
HernandezT, EstrellaI, Perez-GordoM, AlegriaEG, TenorioC, Ruiz-LarrreaF, Moreno-ArribasMV. Contribution of malolactic fermentation by Oenococcus oeni and Lactobacillus plantarum to the changes in the nonanthocyanin polyphenolic composition of red wine. J Agric Food Chem, 2007, 55(13):5260-5266
CrossRef Google scholar
[8]
Hernandez-Valdes JA, van Gestel J, Kuipers OP (2020) A riboswitch gives rise to multi-generational phenotypic heterogeneity in an auxotrophic bacterium. Nat Commun 11(1). https://doi.org/10.1007/10.1038/s41467-020-15017-1
[9]
HuangR, PanM, WanC, ShahNP, TaoX, WeiH. Physiological and transcriptional responses and cross protection of Lactobacillus plantarum ZDY2013 under acid stress. J Dairy Sci, 2016, 99(2):1002-1010
CrossRef Google scholar
[10]
HulloMF, AugerS, DassaE, DanchinA, Martin-VerstraeteI. The metNPQ operon of Bacillus subtilis encodes an ABC permease transporting methionine sulfoxide, D- and L-methionine. Res Microbiol, 2004, 155(2):80-86
CrossRef Google scholar
[11]
InghamSC, HasslerJR, TsaiYW, InghamBH. Differentiation of lactate-fermenting, gas-producing Clostridium spp. isolated from milk. Int J Food Microbiol, 1998, 43(3):173-183
CrossRef Google scholar
[12]
IrvingSE, ChoudhuryNR, CorriganRM. The stringent response and physiological roles of (pp)pGpp in bacteria. Nat Rev Microbiol, 2021, 19(4):256-271
CrossRef Google scholar
[13]
KrielA, BrinsmadeSR, TseJL, TehranchiAK, BittnerAN, SonensheinAL, WangJD. GTP dysregulation in Bacillus subtilis cells lacking (p)ppGpp results in phenotypic amino acid auxotrophy and failure to adapt to nutrient downshift and regulate biosynthesis genes. J Bacteriol, 2014, 196(1):189-201
CrossRef Google scholar
[14]
LiQ, TaoQ, TeixeiraJS, Shu-Wei SuM, GanzleMG. Contribution of glutaminases to glutamine metabolism and acid resistance in Lactobacillus reuteri and other vertebrate host adapted lactobacilli. Food Microbiol, 2020, 86: 103343
CrossRef Google scholar
[15]
LieberCS, PackerL. S-adenosylmethionine: molecular, biological, and clinical aspects - an introduction. Am J Clin Nutr, 2002, 76(5):1148s-1150s
CrossRef Google scholar
[16]
LiuM, PrakashC, NautaA, SiezenRJ, FranckeC. Computational analysis of cysteine and methionine metabolism and its regulation in dairy starter and related bacteria. J Bacteriol, 2012, 194(13):3522-3533
CrossRef Google scholar
[17]
LiuS, LiK, YangS, TianS, HeL. Development of a SCAR (sequence-characterised amplified region) marker for acid resistance-related gene in Lactobacillus plantarum. Extremophiles, 2015, 19(2):355-361
CrossRef Google scholar
[18]
LivakKJ, SchmittgenTD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(−Delta Delta C) method. Methods, 2001, 25(4):402-408
CrossRef Google scholar
[19]
Lombardi SJ, Pannella G, Iorizzo M, Testa B, Succi M, Tremonte P, Sorrentino E, Di Renzo M, Strollo D, Coppola R (2020) Inoculum strategies and performances of malolactic starter Lactobacillus plantarum M10: impact on chemical and sensorial characteristics of Fiano wine. Microorganisms 8(4). https://doi.org/10.1007/10.3390/microorganisms8040516
[20]
LucioO, PardoI, HerasJM, Krieger-WeberS, FerrerS. Use of starter cultures of Lactobacillus to induce malolactic fermentation in wine. Aust J Grape Wine R, 2017, 23(1):15-21
CrossRef Google scholar
[21]
LundP, TramontiA, BiaseDD. Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev, 2014, 38(6):1091-1125
CrossRef Google scholar
[22]
MarkkinenN, LaaksonenO, NahkuR, KuldjarvR, YangB. Impact of lactic acid fermentation on acids, sugars, and phenolic compounds in black chokeberry and sea buckthorn juices. Food Chem, 2019, 286: 204-215
CrossRef Google scholar
[23]
MarkkinenN, PariyaniR, JokiojaJ, KortesniemiM, LaaksonenO, YangB. NMR-based metabolomics approach on optimization of malolactic fermentation of sea buckthorn juice with Lactiplantibacillus plantarum. Food Chem, 2022, 366: 130630
CrossRef Google scholar
[24]
MengQ, YuanY, LiY, WuS, ShiK, LiuS. Optimization of electrotransformation parameters and engineered promoters for Lactobacillus plantarum from wine. ACS Synth Biol, 2021, 10(7):1728-1738
CrossRef Google scholar
[25]
Muhialdin BJ, Kadum H, Hussin ASM (2021) Metabolomics profiling of fermented cantaloupe juice and the potential application to extend the shelf life of fresh cantaloupe juice for six months at 8 °C. Food Control 120. https://doi.org/10.1007/10.1016/j.foodcont.2020.107555
[26]
Muhialdin BJ, Kadum H, Zarei M, Hussin ASM (2020) Effects of metabolite changes during lacto-fermentation on the biological activity and consumer acceptability for dragon fruit juice. LWT-Food Sci Technol 121. https://doi.org/10.1007/10.1016/j.lwt.2019.108992
[27]
Qi Y, Wang H, Chen X, Wei G, Tao S, Fan M (2021) Altered metabolic strategies: elaborate mechanisms adopted by Oenococcus oeni in response to acid stress. J Agric Food Chem. https://doi.org/10.1007/10.1021/acs.jafc.0c07599
[28]
RodionovDA, VitreschakAG, MironovAA, GelfandMS. Comparative genomics of the methionine metabolism in Gram-positive bacteria: a variety of regulatory systems. Nucleic Acids Res, 2004, 32(11):3340-3353
CrossRef Google scholar
[29]
RysselM, HviidAM, DawishMS, HaaberJ, HammerK, MartinussenJ, KilstrupM. Multi-stress resistance in Lactococcus lactis is actually escape from purine-induced stress sensitivity. Microbiology (Reading), 2014, 160(Pt 11):2551-2559
CrossRef Google scholar
[30]
SongX, HuangH, XiongZ, AiL, YangS. CRISPR-Cas9D10A nickase-assisted genome editing in Lactobacillus casei. Appl Environ Microbiol, 2017, 83(22):e01259-e01217
CrossRef Google scholar
[31]
SunSY, GongHS, LiuWL, JinCW. Application and validation of autochthonous Lactobacillus plantarum starter cultures for controlled malolactic fermentation and its influence on the aromatic profile of cherry wines. Food Microbiol, 2016, 55: 16-24
CrossRef Google scholar
[32]
TeixeiraJS, SeerasA, Sanchez-MaldonadoAF, ZhangCG, SuMSW, GanzleMG. Glutamine, glutamate, and arginine-based acid resistance in Lactobacillus reuteri. Food Microbiol, 2014, 42: 172-180
CrossRef Google scholar
[33]
TiitinenK, VahvaselkaM, LaaksoS, KallioH. Malolactic fermentation in four varieties of sea buckthorn (Hippophae rhamnoides L.). Eur Food Res Technol, 2007, 224(6):725-732
CrossRef Google scholar
[34]
Tomita S, Saito K, Nakamura T, Sekiyama Y, Kikuchi J (2017) Rapid discrimination of strain-dependent fermentation characteristics among Lactobacillus strains by NMR-based metabolomics of fermented vegetable juice. PLoS One 12(7). https://doi.org/10.1007/10.1371/journal.pone.0182229
[35]
VeithN, SolheimM, van GrinsvenKWA, OlivierBG, LeveringJ, GrosseholzR, HugenholtzJ, HoloH, NesI, TeusinkB, KummerU. Using a genome-scale metabolic model of Enterococcus faecalis V583 to assess amino acid uptake and its impact on central metabolism. Appl Environ Microbiol, 2015, 81(5):1622-1633
CrossRef Google scholar
[36]
Virdis C, Sumby K, Bartowsky E, Jiranek V (2021) Lactic acid bacteria in wine: technological advances and evaluation of their functional role. Front Microbiol 11. https://doi.org/10.1007/10.3389/fmicb.2020.612118
[37]
WangJF, HeL, AnW, YuDL, LiuSW, ShiK. Lyoprotective effect of soluble extracellular polymeric substances from Oenococcus oeni during its freeze-drying process. Process Biochem, 2019, 84: 205-212
CrossRef Google scholar
[38]
Wu H, Xue E, Zhi N, Song Q, Tian K, Caiyin Q, Yuan L, Qiao J (2020) d-Methionine and d-Phenylalanine improve Lactococcus lactis F44 acid resistance and nisin yield by governing cell wall remodeling. Appl Environ Microbiol 86(9). https://doi.org/10.1007/10.1128/AEM.02981-19
[39]
WuQ, ShahNP. Comparative mRNA-Seq analysis reveals the improved EPS production machinery in Streptococcus thermophilus ASCC 1275 during optimized milk fermentation. Front Microbiol, 2018, 9: 445
CrossRef Google scholar
[40]
WuthrichD, IrmlerS, BerthoudH, GuggenbuhlB, EugsterE, BruggmannR. Conversion of methionine to cysteine in Lactobacillus paracasei depends on the highly mobile cysK-ctl-cysE gene cluster. Front Microbiol, 2018, 9: 2415
CrossRef Google scholar
[41]
WuthrichD, WenzelC, BavanT, BruggmannR, BerthoudH, IrmlerS. Transcriptional regulation of cysteine and methionine metabolism in Lactobacillus paracasei FAM18149. Front Microbiol, 2018, 9: 1261
CrossRef Google scholar
[42]
Xu Y, Zhao Z, Tong WH, Ding YM, Liu B, Shi YX, Wang JC, Sun SM, Liu M, Wang YH, Qi QS, Xian M, Zhao G (2020) An acid-tolerance response system protecting exponentially growing Escherichia coli. Nat Commun 11(1). https://doi.org/10.1007/10.1038/s41467-020-15350-5
[43]
Yang HR, Yu YJ, Fu CX, Chen FS (2019) Bacterial acid resistance toward organic weak acid revealed by RNA-Seq transcriptomic analysis in Acetobacter pasteurianus. Front Microbiol 10. https://doi.org/10.1007/10.3389/fmicb.2019.01616
[44]
ZhangZ, FeigeJN, ChangAB, AndersonIJ, BrodianskiVM, VitreschakAG, GelfandMS Jr, SaierMH. A transporter of Escherichia coli specific for L- and D-methionine is the prototype for a new family within the ABC superfamily. Arch Microbiol, 2003, 180(2):88-100
CrossRef Google scholar
[45]
ZhaoM, LiuS, HeL, TianY. Draft genome sequence of Lactobacillus plantarum XJ25 isolated from Chinese red wine. Genome Announc, 2016, 4(6):e01216
CrossRef Google scholar
[46]
ZhaoN, XuJ, JiaoL, LiuM, ZhangT, LiJ, WeiX, FanM. Acid adaptive response of Alicyclobacillus acidoterrestris: a strategy to survive lethal heat and acid stresses. Food Res Int, 2022, 157: 111364
CrossRef Google scholar
Funding
National Natural Science Foundation of China(32072206); National Key R&D Program of China(2019YFD1002503); China Technology Agriculture Research System(CARS-29-jg-3)

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