Abstract
As the important functional microorganism in the brewing process of Chinese Baijiu, lactic acid bacteria influences the microbial community and production of flavor substances in the Baijiu brewing process. In this study, we first isolated an Acetilactobacillus **shanensis strain from baijiu fermented grains and named it A. **shanensis BJ01. Its optimal growth conditions are 30 °C and pH 3.5. In particular, A. **shanensis BJ01 cannot utilize inorganic acids and most organic acids, except for lactic acid (HL) and acetic acid (HAc). The observed phenotypes showed good growth with HL. When the mixed acid of HL–HAc (V:V = 1:1) was used, the growth rate of A. **shanensis BJ01 greatly accelerated. Transcriptomic sequencing revealed the specific responses of the strain to the acidulants used. The number of upregulated genes in HL–HAc medium was more than that in single acid medium (HL or HAc). KEGG enrichment analyses indicated that the glycometabolism level of HAc regulation was relatively downregulated. The gene expression of quorum sensing and ABC transporter pathways were remarkably upregulated under HL–HAc regulation. Pyruvate metabolic pathway may be an important reason for the difference in A. **shanensis BJ01 response to different organic acids. Our study reported a new organic acid-inducible growth type of bacteria mainly depending on the presence of HL and HAc, and was beneficial to the improvement of fermentation technology of Baijiu.
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Data availability
The RNA-seq data discussed in this study have been deposited in National Center for Biotechnology Information (NCBI) with accession number PRJNA886850.
References
Gong M, Zhou Z, Liu S, Zhu S, Li G, Zhong F, Mao J (2021) Formation pathways and precursors of furfural during Zhenjiang aromatic vinegar production. Food Chem 354:129503. https://doi.org/10.1016/j.foodchem.2021.129503
Illeghems K, De Vuyst L, Weckx S (2015) Comparative genome analysis of the candidate functional starter culture strains Lactobacillus fermentum 222 and Lactobacillus plantarum 80 for controlled cocoa bean fermentation processes. BMC Genomics 16:1–13. https://doi.org/10.1186/s12864-015-1927-0
Jiang H, Lei R, Ding SW, Zhu S (2014) Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinform 15:182. https://doi.org/10.1186/1471-2105-15-182
Krell T, Lacal J, Busch A, Silva-Jimenez H, Guazzaroni ME, Ramos JL (2010) Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 64:539–559. https://doi.org/10.1146/annurev.micro.112408.134054
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Li W, Yang L, Nan W, Lu J, Zhang S, Ujiroghene OJ, Pang X, Lv J (2020) Whole-genome sequencing and genomic-based acid tolerance mechanisms of Lactobacillus delbrueckii subsp. Bulgaricus LJJ Appl Microbiol Biotechnol 104:7631–7642. https://doi.org/10.1007/s00253-020-10788-5
Liu PL, Miao LH (2020) Multiple batches of fermentation promote the formation of functional microbiota in chinese miscellaneous-flavor Baijiu fermentation. Front Microbiol 11:75. https://doi.org/10.3389/fmicb.2020.00075
Liu J, Li L, Peters BM, Li B, Chen L, Deng Y, Xu Z, Shirtliff ME (2017) The viable but nonculturable state induction and genomic analyses of Lactobacillus casei BM-LC14617, a beer-spoilage bacterium. Microbiologyopen 6:e00506. https://doi.org/10.1002/mbo3.506
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Ma R, Sui L, Zhang J, Hu J, Liu P (2019) Polyphasic characterization of yeasts and lactic acid bacteria metabolic contribution in semi-solid fermentation of Chinese baijiu (traditional fermented alcoholic drink): towards the design of a tailored starter culture. Microorganisms 7:147. https://doi.org/10.3390/microorganisms7050147
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugars. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Mols M, van Kranenburg R, Tempelaars MH, van Schaik W, Moezelaar R, Abee T (2010) Comparative analysis of transcriptional and physiological responses of Bacillus cereus to organic and inorganic acid shocks. Int J Food Microbiol 137:13–21. https://doi.org/10.1016/j.ijfoodmicro.2009.09.027
Pang X, Han B, Huang X, Zhang X, Hou L, Cao M, Gao L, Hu G, Chen J (2018) Effect of the environment microbiota on the flavour of light-flavour Baijiu during spontaneous fermentation. Scientific Rep 8:1–12. https://doi.org/10.1038/s41598-018-21814-y
Peng J, Miao L, Chen X, Liu P (2018) Comparative transcriptome analysis of Pseudomonas putida KT2440 revealed its response mechanisms to elevated levels of zinc stress. Front Microbiol 9:1669. https://doi.org/10.3389/fmicb.2018.01669
Pieterse B, Leer RJ, Schuren FH, van der Werf MJ (2005) Unravelling the multiple effects of lactic acid stress on Lactobacillus plantarum by transcription profiling. Microbiology 151:3881–3894. https://doi.org/10.1099/mic.0.28304-0
Song Z, Du H, Zhang Y, Xu Y (2017) Unraveling core functional microbiota in traditional solid-state fermentation by high-throughput amplicons and metatranscriptomics sequencing. Front Microbiol 8:1294–1307. https://doi.org/10.3389/fmicb.2017.01294
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Tan Y, Zhong H, Zhao D, Du H, Xu Y (2019) Succession rate of microbial community causes flavor difference in strong-aroma Baijiu making process. Int J Food Microbiol 311:108350. https://doi.org/10.1016/j.ijfoodmicro.2019.108350
Tsujikawa Y, Ishikawa S, Sakane I, Yoshida KI, Osawa R (2021) Identification of genes encoding a novel ABC transporter in Lactobacillus delbrueckii for inulin polymers uptake. Sci Rep-UK 11:1–12. https://doi.org/10.1038/s41598-021-95356-1
Yu Y, Li X, Zhang J, Chai L, Lu Z, Xu Z (2020) Lactobacillus **shani sp. nov., isolated from solid-state vinegar culture of Zhenjiang aromatic vinegar. Antonie Van Leeuwenhoek 113:43–54. https://doi.org/10.1007/s10482-019-01316-1
Yuan S, ** Z, Ali A, Wang C, Liu J (2022) Caproic acid-producing bacteria in Chinese Baijiu brewing. Front Microbiol 13:883142. https://doi.org/10.3389/fmicb.2022.883142
Zhang J, Fang F, Chen J, Du G (2014) The arginine deiminase pathway of koji bacteria is involved in ethyl carbamate precursor production in soy sauce. FEMS Microbiol Lett 358:91–97. https://doi.org/10.1111/1574-6968.12542
Zheng J, Wittouck S, Salvetti E, Franz CMAP, Harris HMB, Mattarelli P, O’Toole PW, Pot B, Vandamme P, Walter J, Watanabe K, Wuyts S, Felis GE, Gänzle MG, Lebeer S (2020) A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Micr 70(4):2782–2858. https://doi.org/10.1099/ijsem.0.004107
Zou W, Zhao C, Luo H (2018) Diversity and function of microbial community in Chinese strong-flavor baijiu ecosystem: a review. Front Microbiol 9:671. https://doi.org/10.3389/fmicb.2018.00671
Funding
This research was supported by the Hubei Provincial Natural Science Foundation of China (Grant No. 2019CFB265), and the Science and Technology Innovation Project 2020 of Hubei Baiyunbian baijiu Co., Ltd.
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WFL and LHM conceived and designed the experiments. YPL, YZ, and YBY performed the experiments. WFL, YPL, and LHM analyzed the data. TYY contributed materials. WFL wrote the paper.
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Communicated by Yusuf Akhter.
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Liao, W., Li, Y., Zhang, Y. et al. Comparative analysis of the transcriptional responses of Acetilactobacillus **shanensis BJ01 to organic acids. Arch Microbiol 205, 381 (2023). https://doi.org/10.1007/s00203-023-03715-5
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DOI: https://doi.org/10.1007/s00203-023-03715-5