Cited by 30Fermentation and Sensory AnalysisProbiotics and Fermented FoodsBiochemical and biochemical processes

Metabolomic analysis of the effects of a mixed culture of Saccharomyces cerevisiae and Lactiplantibacillus plantarum on the physicochemical and quality characteristics of apple cider vinegar

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Li, Ya-Nan, Luo, Yue, Lu, Zhen-Ming, Dong, Yan-Lin, Chai, Li-Juan, Shi, Jin-Song, Zhang, Xiao-Juan, Xu, Zheng-Hong·2023·Frontiers in Nutrition

Abstract

Introduction: This study compared differences in physicochemical characteristics of the vinegar made by a mixed culture (MC) of Saccharomyces cerevisiae and Lactiplantibacillus plantarum and a pure culture (PC) of Saccharomyces cerevisiae. Methods: The fermentation process was monitored, and metabolomics analysis by Liquid Chromagraphy-Mass Spectrometry (LC-MS) was applied to the compositional differences between PC and MC vinegars, combined with quantification of organic acids, amino acids and B vitamins. Results: A total of 71 differential metabolites including amino acids, organic acids and carbohydrates, and six possible key metabolic pathways were identified. MC enhanced the malic acid utilization and pyruvate acid metabolism during fermentation, increasing substrate-level phosphorylation, and supplying more energy for cellular metabolism. Higher acidity at the beginning of acetic acid fermentation, resulting from lactic acid production by Lactiplantibacillus plantarum in MC, suppressed the cellular metabolism and growth of Acetobacter pasteurianus, but enhanced its alcohol metabolism and acetic acid production in MC. MC vinegar contained more vitamin B, total flavonoids, total organic acids, amino acids and had a higher antioxidant capacity. MC enhanced the volatile substances, particularly ethyl lactate, ethyl caprate and ethyl caproate, which contributed to a stronger fruity aroma. Discussion: These results indicated the mixed culture in alcoholic fermentation can effectively enhance the flavor and quality of apple cider vinegar.

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  • In fermentation, other low-abundance primary metabolites including glycerol, succinate, acetate, and lactate significantly influence flavor characteristics, enhance the complexity of fermentation products, and are closely associated with yeast metabolic capacity.

    “In the fermentation process, while alcohols play a crucial role in determining the overall flavor profile, other low-abundance primary metabolites also significantly influence flavor characteristics. These metabolites, including glycerol, succinate, acetate, and lactate, not only enhance the complexity of fermentation products but are also closely associated with yeast metabolic capacity [54,57,58”

    From The Metabolic Pathways of Yeast and Acetic Acid Bacteria During Fruit Vinegar Fermentation and Their Influence on Flavor Development (2025) · cites this paper as [58]

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Research works printed but not linked: 47

  1. [1]Alonso AM Castro R Rodriguez MC Guillen DA Barroso CG. Study of the antioxidant power of brandies and vinegars derived from Sherry wines and correlation with their content in polyphenols. Food Res Int. (2004) 37: 715– 21. 10.1016/j.foodres.2004.03.007 · DOI · Paper page
  2. [2]Qi ZL Dong D Yang HL Xia XL. Improving fermented quality of cider vinegar via rational nutrient feeding strategy. Food Chem. (2017) 224: 312– 9. 10.1016/j.foodchem.2016.12.078 28159272 · DOI
  3. [3]Verzelloni E Tagliazucchi D Conte A. Relationship between the antioxidant properties and the phenolic and flavonoid content in traditional balsamic vinegar. Food Chem. (2007) 105: 564– 71. 10.1016/j.foodchem.2007.04.014 · DOI
  4. [4]Wu XF Yao HL Cao XM Liu Q Cao LL Mu DD Production of vinegar from purple sweet potato in a liquid fermentation process and investigation of its antioxidant activity. 3 Biotech. (2017) 7: 308. 10.1007/s13205-017-0939-7 28955605 PMC5595722 · DOI
  5. [5]Xie XL Zheng Y Liu X Cheng C Zhang XL Xia T Antioxidant activity of Chinese Shanxi aged vinegar and its correlation with polyphenols and flavonoids during the brewing process. J Food Sci. (2017) 82: 2479– 86. 10.1111/1750-3841.13914 28898412 · DOI
  6. [7]Wang ZB Li TT Liu FY Zhang CS Ma HL Wang L Effects of ultrasonic treatment on the maturation of Zhenjiang vinegar. Ultrason Sonochem. (2017) 39: 272– 80. 10.1016/j.ultsonch.2017.04.020 28732946 · DOI
  7. [9]Gheflati A Bashiri R Ghadiri-Anari A Reza JZ Kord MT Nadjarzadeh A. The effect of apple vinegar consumption on glycemic indices, blood pressure, oxidative stress, and homocysteine in patients with type 2 diabetes and dyslipidemia: a randomized controlled clinical trial. Clin Nutr Espen. (2019) 33: 132– 8. 10.1016/j.clnesp.2019.06.006 31451249 · DOI
  8. [10]Williams AA Tucknott OG. The volatile aroma components of fermented ciders: minor neutral components from the fermentation of sweet coppin apple juice. J Sci Food Agric. (1978) 29: 381– 97. 10.1002/jsfa.2740290414 · DOI
  9. [12]Huang T Lu ZM Peng MY Liu ZF Chai LJ Zhang XJ Combined effects of fermentation starters and environmental factors on the microbial community assembly and flavor formation of Zhenjiang aromatic vinegar. Food Res Int. (2022) 152: 110900. 10.1016/j.foodres.2021.110900 35181076 · DOI
  10. [13]Wu YF Xia ML Zhao N Tu LN Xue DN Zhang XL Metabolic profile of main organic acids and its regulatory mechanism in solid-state fermentation of Chinese cereal vinegar. Food Res Int. (2021) 145: 110400. 10.1016/j.foodres.2021.110400 34112403 · DOI · Paper page
  11. [14]Callejon RM Morales ML Troncoso AM Ferreira ACS. Targeting key aromatic substances on the typical aroma of Sherry vinegar. J Agric Food Chem. (2008) 56: 6631– 9. 10.1021/jf703636e 18616263 · DOI
  12. [15]Liu YZ Rousseaux S Tourdot-Marechal R Sadoudi M Gougeon R Schmitt-Kopplin P Wine microbiome: a dynamic world of microbial interactions. Crit Rev Food Sci Nutr. (2017) 57: 856– 73. 10.1080/10408398.2014.983591 26066835 · DOI
  13. [16]Wang XW Han MZ Zhang MN Wang Y Ren YP Yue TL In vitro evaluation of the hypoglycemic properties of lactic acid bacteria and its fermentation adaptability in apple juice. Lwt-Food Sci Technol. (2021) 136: 110363. 10.1016/j.lwt.2020.110363 · DOI
  14. [17]Xu Z Lu Z Soteyome T Ye Y Huang T Liu J Polymicrobial interaction between Lactobacillus and Saccharomyces cerevisiae: coexistence-relevant mechanisms. Crit Rev Microbiol. (2021) 47: 386– 96. 10.1080/1040841X.2021.1893265 33663335 · DOI
  15. [18]Jarosz DF Brown JC Walker GA Datta MS Ung WL Lancaster AK Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell. (2014) 158: 1083– 93. 10.1016/j.cell.2014.07.025 25171409 PMC4424051 · DOI
  16. [19]Mendes F Sieuwerts S de Hulster E Almering MJ Luttik MA Pronk JT Transcriptome-based characterization of interactions between Saccharomyces cerevisiae and Lactobacillus delbrueckii subsp. bulgaricus in lactose-grown chemostat cocultures. Appl Environ Microbiol. (2013) 79: 5949– 61. 23872557 PMC3811385
  17. [20]Gerardi C Tristezza M Giordano L Rampino P Perrotta C Baruzzi F Exploitation of Prunus mahaleb fruit by fermentation with selected strains of Lactobacillus plantarum and Saccharomyces cerevisiae. Food Microbiol. (2019) 84: 103262. 10.1016/j.fm.2019.103262 31421756 · DOI
  18. [21]Loh LX Ng DHJ Toh MZ Lu YY Liu SQ. Targeted and nontargeted metabolomics of amino acids and bioactive metabolites in probiotic-fermented unhopped beers using liquid chromatography high-resolution mass spectrometry. J Agric Food Chem. (2021) 69: 14024– 36. 10.1021/acs.jafc.1c03992 34734707 · DOI
  19. [22]Ramirez JE Zambrano R Sepulveda B Kennelly EJ Simirgiotis MJ. Anthocyanins and antioxidant capacities of six Chilean berries by HPLC-HR-ESI-ToF-MS. Food Chem. (2015) 176: 106– 14. 10.1016/j.foodchem.2014.12.039 25624212 · DOI
  20. [23]Tao Y Sun DW Gorecki A Blaszczak W Lamparski G Amarowicz R A preliminary study about the influence of high hydrostatic pressure processing in parallel with oak chip maceration on the physicochemical and sensory properties of a young red wine. Food Chem. (2016) 194: 545– 54. 10.1016/j.foodchem.2015.07.041 26471591 · DOI
  21. [24]Wang Z Feng Y Yang N Jiang T Xu H Lei H. Fermentation of kiwifruit juice from two cultivars by probiotic bacteria: bioactive phenolics, antioxidant activities and flavor volatiles. Food Chem. (2022) 373: 131455. 10.1016/j.foodchem.2021.131455 34731808 · DOI
  22. [25]Li HC Huang JT Wang YQ Wang XN Ren YC Yue TL Study on the nutritional characteristics and antioxidant activity of dealcoholized sequentially fermented apple juice with Saccharomyces cerevisiae and Lactobacillus plantarum fermentation. Food Chem. (2021) 363: 130351. 10.1016/j.foodchem.2021.130351 34147897 · DOI
  23. [26]Natić MM Dabić DČ Papetti A Akšić MMF Ognjanov V Ljubojević M Analysis and characterisation of phytochemicals in mulberry (Morus alba L.) fruits grown in Vojvodina, North Serbia. Food Chem. (2015) 171: 128– 136. 10.1016/j.foodchem.2014.08.101 25308652 · DOI
  24. [27]Kwaw E Ma YK Tchabo W Apaliya MT Wu M Sackey AS Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice. Food Chem. (2018) 250: 148– 54. 10.1016/j.foodchem.2018.01.009 29412905 · DOI
  25. [28]Li ZX Teng J Lyu YL Hu XQ Zhao YL Wang MF. Enhanced antioxidant activity for apple juice fermented with Lactobacillus plantarum ATCC14917. Molecules. (2019) 24: 51. 10.3390/molecules24010051 30586844 PMC6337214 · DOI
  26. [29]Li TL Jiang T Liu N Wu CY Xu HD Lei HJ. Biotransformation of phenolic profiles and improvement of antioxidant capacities in jujube juice by select lactic acid bacteria. Food Chem. (2021) 339: 127859. 10.1016/j.foodchem.2020.127859 32829244 · DOI
  27. [30]Luciano WA Matte TC Portela IA de Medeiros LL Lima MD Maciel JF Effects of Lactobacillus acidophilus LA-3 on physicochemical and sensory parameters of acai and mango based smoothies and its survival following simulated gastrointestinal conditions. Food Res Int. (2018) 114: 159– 68. 10.1016/j.foodres.2018.08.005 30361012 · DOI
  28. [31]Schreckinger ME Wang JZ Yousef G Lila MA de Mejia EG. Antioxidant capacity and in vitro inhibition of adipogenesis and inflammation by phenolic extracts of vaccinium floribundum and aristotelia chilensis. J Agric Food Chem. (2010) 58: 8966– 76. 10.1021/jf100975m 23654232 · DOI
  29. [32]Dunn WB Broadhurst D Begley P Zelena E Francis-McIntyre S Anderson N Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc. (2011) 6: 1060– 83. 10.1038/nprot.2011.335 21720319 · DOI · Paper page
  30. [33]Sangster T Major H Plumb R Wilson AJ Wilson ID. A pragmatic and readily implemented quality control strategy for HPLC-MS and GC-MS-based metabonomic analysis. Analyst. (2006) 131: 1075– 8. 10.1039/B604498K 17003852 · DOI
  31. [34]Zelena E Dunn WB Broadhurst D Francis-McIntyre S Carroll KM Begley P Development of a robust and repeatable UPLC- MS method for the long-term metabolomic study of human serum. Anal Chem. (2009) 81: 1357– 64. 10.1021/ac8019366 19170513 · DOI
  32. [35]Heires MJNPE. The international organization for standardization (ISO). New Polit Econ. (2008) 13: 357– 367. 10.1080/13563460802302693 · DOI
  33. [36]Park MK Kim Y-S. Comparative metabolic expressions of fermented soybeans according to different microbial starters. Food Chem. (2020) 305: 125461. 10.1016/j.foodchem.2019.125461 31505412 · DOI
  34. [38]Gomes RJ de Fatima Borges M de Freitas Rosa M Castro-Gómez RJH Spinosa WA. Acetic acid bacteria in the food industry: systematics, characteristics and applications. Food Technol Biotechnol. (2018) 56: 139. 10.17113/ftb.56.02.18.5593 30228790 PMC6117990 · DOI
  35. [39]Chen Y Bai Y Li D Wang C Xu N Wu S Correlation between ethanol resistance and characteristics of PQQ-dependent ADH in acetic acid bacteria. Eur Food Res Technol. (2016) 242: 837– 47. 10.1007/s00217-015-2589-5 · DOI
  36. [40]Trček J Mira NP Jarboe LR. Adaptation and tolerance of bacteria against acetic acid. Appl Microbiol Biotechnol. (2015) 99: 6215– 6229. 10.1007/s00253-015-6762-3 26142387 · DOI
  37. [41]Saichana N Matsushita K Adachi O Frébort I Frebortova J. Acetic acid bacteria: a group of bacteria with versatile biotechnological applications. Biotechnol Adv. (2015) 33: 1260– 71. 10.1016/j.biotechadv.2014.12.001 25485864 · DOI
  38. [43]Gan RY Shah NP Wang MF Lui WY Corke HJ. Lactobacillus plantarum WCFS1 fermentation differentially affects antioxidant capacity and polyphenol content in mung bean (Vigna radiata) and soya bean (Glycine max) milks. J Food Proces Preserv. (2017) 41: e12944. 10.1111/jfpp.12944 · DOI
  39. [44]Jurgenson CT Begley TP Ealick SEJ. The structural and biochemical foundations of thiamin biosynthesis. Annu Rev Biochem. (2009) 78: 569. PMC6078420 19348578
  40. [45]Leonardi R Jackowski S. Biosynthesis of pantothenic acid and coenzyme A. EcoSal Plus. (2007) 2:10.1128/ecosalplus.3.6.3.4. 10.1128/ecosalplus.3.6.3.4 26443589 PMC4950986 · DOI
  41. [49]Huang A Jiang Z Tao M Wen M Xiao Z Zhang L Targeted and nontargeted metabolomics analysis for determining the effect of storage time on the metabolites and taste quality of keemun black tea. Food Chem. (2021) 359: 129950. 10.1016/j.foodchem.2021.129950 33945989 · DOI
  42. [50]Zhang X Zheng YR Feng J Zhou R Ma M. Integrated metabolomics and high-throughput sequencing to explore the dynamic correlations between flavor related metabolites and bacterial succession in the process of Mongolian cheese production. Food Res Int. (2022) 160: 111672. 10.1016/j.foodres.2022.111672 36076384 · DOI
  43. [51]Zhao M Zhang H Wang JM Shan DD Xu Q. Serum metabolomics analysis of the intervention effect of whole grain oats on insulin resistance induced by high-fat diet in rats. Food Res Int. (2020) 135: 109297. 10.1016/j.foodres.2020.109297 32527488 · DOI
  44. [52]Graulet B. Improving the level of vitamins in milk. In: Griffiths MW editor. Improving the safety and quality of milk. Amsterdam: Elsevier (2010). p. 229– 51.
  45. [53]Ashihara H Yin Y Katahira R Watanabe S Mimura T Sasamoto H. Comparison of the formation of nicotinic acid conjugates in leaves of different plant species. Plant Physiol Biochem. (2012) 60: 190– 5. 10.1016/j.plaphy.2012.08.007 22983143 · DOI
  46. [54]Carlson LA. Nicotinic acid: the broad-spectrum lipid drug. A 50th anniversary review. J Intern Med. (2005) 258: 94– 114. 10.1111/j.1365-2796.2005.01528.x 16018787 · DOI
  47. [55]Sun SY Gong HS Liu WL Jin CW. 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. 10.1016/j.fm.2015.11.016 26742612 · DOI

Cited by

Sorted by citations

Authors
Li, Y.-N., Luo, Y., Lu, Z.-M., Dong, Y.-L., Chai, L.-J., Shi, J.-S., Zhang, X.-J., & Xu, Z.-H.
Affiliations
Jiangnan University (CN)
Venue
Frontiers in Nutrition
Published
2023-03-14
Volume
10
Pages
1142517-1142517
ISSN
2296-861X (ISSN-L)
OpenAlex
W4324146064
Cited by
30
References
2
Citations by year
2026: 4 · 2025: 10 · 2024: 10 · 2023: 6
FWCI
4.33
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Nutrition (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Biochemical and biochemical processes
Keywords
apple cider vinegar, Saccharomyces cerevisiae, Lactobacillus plantarum, mixed culture fermentation, acetic acid fermentation, Acetobacter pasteurianus, pyruvate metabolism, lactic acid production, organic acids, amino acids, B vitamins, volatile compounds, ethyl lactate, antioxidant capacity, vinegar flavor

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