The bacterial succession and its role in flavor compounds formation during the fermentation of cigar tobacco leaves

Hongyang Si , Kun Zhou , Tingyi Zhao , Bing Cui , Fang Liu , Mingqin Zhao

Bioresources and Bioprocessing ›› 2023, Vol. 10 ›› Issue (1) : 74

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Bioresources and Bioprocessing ›› 2023, Vol. 10 ›› Issue (1) : 74 DOI: 10.1186/s40643-023-00694-9
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The bacterial succession and its role in flavor compounds formation during the fermentation of cigar tobacco leaves

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Abstract

Fermentation is the key process required for developing the characteristic properties of cigar tobacco leaves, complex microorganisms are involved in this process. However, the microbial fermentation mechanisms during the fermentation process have not been well-characterized. This study investigated the dynamic changes in conventional chemical composition, flavor compounds, and bacterial community during the fermentation of cigar tobacco leaves from Hainan and Sichuan provinces in China, as well as the potential roles of bacteria. Fermentation resulted in a reduction of conventional chemical components in tobacco leaves, with the exception of a noteworthy increase in insoluble protein content. Furthermore, the levels of 10 organic acids and 19 amino acids showed a significant decrease, whereas the concentration of 30 aromatic substances exhibited a unimodal trend. Before fermentation, the bacterial community structures and dominant bacteria in Hainan and Sichuan tobacco leaves differed significantly. As fermentation progressed, the community structures in the two regions became relatively similar, with Delftia, Ochrobactrum, Rhodococcus, and Stenotrophomonas being dominant. Furthermore, a total of 12 functional bacterial genera were identified in Hainan and Sichuan tobacco leaves using bidirectional orthogonal partial least squares (O2PLS) analysis. Delftia, Ochrobactrum, and Rhodococcus demonstrated a significant negative correlation with oleic acid and linoleic acid, while Stenotrophomonas and Delftia showed a significant negative correlation with undesirable amino acids, such as Ala and Glu. In addition, Bacillus showed a positive correlation with benzaldehyde, while Kocuria displayed a positive correlation with 2-acetylfuran, isophorone, 2, 6-nonadienal, and β-damascenone. The co-occurrence network analysis of microorganisms revealed a prevalence of positive correlations within the bacterial network, with non-abundant bacteria potentially contributing to the stabilization of the bacterial community. These findings can improve the overall tobacco quality and provide a novel perspective on the utilization of microorganisms in the fermentation of cigar tobacco leaves.

Keywords

Cigar tobacco leaves / Fermentation / Bacterial community / Flavor substances / Co-occurrence network

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Hongyang Si, Kun Zhou, Tingyi Zhao, Bing Cui, Fang Liu, Mingqin Zhao. The bacterial succession and its role in flavor compounds formation during the fermentation of cigar tobacco leaves. Bioresources and Bioprocessing, 2023, 10(1): 74 DOI:10.1186/s40643-023-00694-9

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References

[1]

Ali H, Paetzold R, Brueckner H. Determination of L- and D-amino acids in smokeless tobacco products and tobacco. Food Chem, 2006, 99: 803-812.

[2]

Bhat SV, Maughan H, Cameron ADS, Yost CK. Phylogenomic analysis of the genus Delftia reveals distinct major lineages with ecological specializations. Microb Genom, 2022

[3]

Centeno JA, Garabal JI, Docampo F, Lorenzo JM, Carballo J. Recovering traditional raw-milk Tetilla cheese flavour and sensory attributes by using Kocuria varians and Yarrowia lipolytica adjunct cultures. Int J Food Microbiol, 2017, 251: 33-40.

[4]

Chen X, Zhao X, Ge J, Zhao Y, Zhao R. Recognition of the neutral sugars conversion induced by bacterial community during lignocellulose wastes composting. Bioresour Technol, 2019, 294: 122153.

[5]

Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13: 1194-1202.

[6]

Chen Y, Zhang W, Yi H, Wang B, Xiao J, Zhou X, Xu J, Jiang L, Shi X. Microbial community composition and its role in volatile compound formation during the spontaneous fermentation of ice wine made from Vidal grapes. Process Biochem, 2020, 92: 365-377.

[7]

Chen J, Li Y, He X, Jiao F, Zou C. Influences of different curing methods on chemical compositions in different types of tobaccos. Ind Crops Prod, 2021, 167: 113534.

[8]

Dai J, Dong A, Xiong G, Liu Y, Qiu D. Production of highly active extracellular amylase and cellulase from Bacillus subtilis ZIM3 and a recombinant strain with a potential application in tobacco fermentation. Front Microbiol, 2020, 11: 1539.

[9]

Deng Y, Jiang YH, Yang Y, He Z, Luo F, Zhou J. Molecular ecological network analyses. BMC Bioinf, 2012, 13: 113.

[10]

Deng X, Huang G, Tu Q, Zhou H, Li Y, Shi H, Wu X, Ren H, Huang K, He X, Xu W. Evolution analysis of flavor-active compounds during artificial fermentation of Pu-erh tea. Food Chem, 2021

[11]

Di Giacomo M, Paolino M, Silvestro D, Vigliotta G, Imperi F, Visca P, Alifano P, Parente D. Microbial community structure and dynamics of dark fire-cured tobacco fermentation. Appl Environ Microbiol, 2007, 73: 825-837.

[12]

Ding S, Tian M, Pan Y, Suo L, Zhu X, Ren D, Yu H. Diversity and dynamics of microbial population during fermentation of gray sufu and their correlation with quality characteristics. Lebensm Wiss Technol, 2023

[13]

Du H, Wang X, Zhang Y, Xu Y. Exploring the impacts of raw materials and environments on the microbiota in Chinese Daqu starter. Int J Food Microbiol, 2019, 297: 32-40.

[14]

Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods, 2013, 10: 996.

[15]

El Bouhaddani S, Houwing-Duistermaat J, Salo P, Perola M, Jongbloed G, Uh H. Evaluation of O2PLS in omics data integration. BMC Bioinf, 2016

[16]

Fan J, Kong G, Yao H, Wu Y, Zhao G, Li F, Zhang G. Widely targeted metabolomic analysis reveals that volatile metabolites in cigar tobacco leaves dynamically change during fermentation. Biochem Biophys Rep, 2023, 35: 101532-101532.

[17]

Feng K, Peng X, Zhang Z, Gu S, He Q, Shen W, Wang Z, Wang D, Hu Q, Li Y, Wang S, Deng Y. iNAP: an integrated network analysis pipeline for microbiome studies. iMeta, 2022

[18]

Frankenburg WG. Transformation products of nicotine in fermented tobacco. Science, 1948, 107: 427-428.

[19]

Frankenburg WG. Chemical changes in the harvested tobacco leaf advances in enzymology and related areas of molecular biology, 1950, New York: Wiley.

[20]

Frankenburg WG, Gottscho AM. Nitrogen compounds in fermented cigar leaves. Ind Eng Chem, 1952, 44: 301-305.

[21]

Gaines TP, Miles JD. Protein composition and classification of tobacco. J Agric Food Chem, 1975, 23: 690-694.

[22]

Giraffa G, Neviani E. DNA-based, culture-independent strategies for evaluating microbial communities in food-associated ecosystems. Int J Food Microbiol, 2001, 67: 19-34.

[23]

Gong X, Ma G, Duan Y, Zhu D, Chen Y, Zhang K, Yang J. Biodegradation and metabolic pathway of nicotine in Rhodococcus sp Y22. World J Microbiol Biotechnol, 2016

[24]

Guan Q, Huang T, Peng F, Huang J, Liu Z, Peng Z, Xie M, Xiong T. The microbial succession and their correlation with the dynamics of flavor compounds involved in the natural fermentation of suansun, a traditional Chinese fermented bamboo shoots. Food Res Int, 2022

[25]

Guan T, Wu X, Hou R, Tian L, Huang Q, Zhao F, Liu Y, Jiao S, Xiang S, Zhang J, Li D, Luo J, Jin Z, He Z. Application of Clostridium butyricum, Rummeliibacillus suwonensis, and Issatchenkia orientalis for Nongxiangxing baijiu fermentation: Improves the microbial communities and flavor of upper fermented grain. Food Res Int, 2023

[26]

Gunina A, Kuzyakov Y. Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem, 2015, 90: 87-100.

[27]

Guo W, Guo J, Dong H, Xu L, Han J, Liu W, Wang T, Zhuang S, Zhang Y, Mou W. Correlation between free amino acids and smoking quality of flue-cured tobacco and variations during flue-curing process. Acta Tabacaria Sinica, 2018, 24: 16-25.

[28]

Hamilton JL, Lowe RH. Changes in the concentration of proteins, amino acids and ammonia in burley tobacco during air curing. Tob Sci, 1978, 22: 89-93.

[29]

Hu H, Xu Z, Su Y, Chen Y, Wang X. Research progress in factors influencing nephytadiene content in tobacco leaves. Acta Agriculture Jiangxi, 2010, 22: 17-20.

[30]

Hu H, Liu Y, Huang Y, Zhang Z, Tang H. The leaf microbiome of tobacco plants across eight Chinese provinces. Microorganisms, 2022

[31]

Hu W, Cai W, Zheng Z, Liu Y, Luo C, Xue F, Li D. Study on the chemical compositions and microbial communities of cigar tobacco leaves fermented with exogenous additive. Sci Rep, 2022

[32]

Hu W, Zhou Q, Cai W, Liu J, Li P, Hu D, Luo C, Li D. Effects of coffee and cocoa as fermentation additives on sensory quality and chemical compositions of cigar tobacco leaves. Cienc Technol Aliment, 2023

[33]

Huang W, Zhang C, Gu Z, Li C, Fang Z, Zeng Z, Zhang Z, Hu B, Chen H, Wu W, Wang T, Lan X, Liu Y. Effect of microbial fermentation on the sensory characteristics and chemical compositions of Chinese sweet tea (Lithocarpus litseifolius (Hance) Chun). Food Biosci, 2022

[34]

Hughes AR, Inouye BD, Johnson MTJ, Underwood N, Vellend M. Ecological consequences of genetic diversity. Ecol Lett, 2008, 11: 609-623.

[35]

Jia Y, Liu Y, Hu W, Cai W, Zheng Z, Luo C, Li D. Development of Candida autochthonous starter for cigar fermentation via dissecting the microbiome. Front Microbiol, 2023

[36]

Jiang C, Liu Y, Li H, Zhu S, Sun X, Wu K, Shui W. The characterization of microbial communities and associations in karst tiankeng. Front Microbiol, 2022

[37]

Jin M, Chen Y, Wu Y, Yang W, He Z, Zhao M. Effects of drying temperature on nitrogen transformation mechanism of cigar tobacco during discoloration period. Crops, 2023, 1: 76-83.

[38]

Juarez-Jimenez B, Manzanera M, Rodelas B, Victoria Martinez-Toledo M, Gonzalez-Lopez J, Crognale S, Pesciaroli C, Fenice M. Metabolic characterization of a strain (BM90) of Delftia tsuruhatensis showing highly diversified capacity to degrade low molecular weight phenols. Biodegradation, 2010, 21: 475-489.

[39]

Koilybayeva M, Shynykul Z, Ustenova G, Abzaliyeva S, Alimzhanova M, Amirkhanova A, Turgumbayeva A, Mustafina K, Yeleken G, Raganina K, Kapsalyamova E. Molecular characterization of some Bacillus species from vegetables and evaluation of their antimicrobial and antibiotic potency. Molecules, 2023

[40]

Kou M, Wang C, Dai Y, Zeng D, Jia Y. Analysis on free amino in cigar tobacco of different habitats and grades. Southwest China J Agric Sci, 2013, 26: 963-967.

[41]

Kuang X, Su H, Li W, Lin L, Lin W, Luo L. Effects of microbial community structure and its co-occurrence on the dynamic changes of physicochemical properties and free amino acids in the cantonese soy sauce fermentation process. Food Res Int, 2022

[42]

Li Q, Li Y, Luo Y, Zhang Y, Chen Y, Lin H, Wang K, Huang J, Liu Z. Shifts in diversity and function of the bacterial community during the manufacture of Fu brick tea. Food Microbiol, 2019, 80: 70-76.

[43]

Li J, Zhao Y, Qin Y, Shi H. Influence of microbiota and metabolites on the quality of tobacco during fermentation. BMC Microbiol, 2020

[44]

Li Y, Li W, Li C, Li L, Yang D, Wang Y, Chen S, Wang D, Wu Y. Novel insight into flavor and quality formation in naturally fermented low-salt fish sauce based on microbial metabolism. Food Res Int, 2023

[45]

Liang L, Ma Y, Jiang Z, Sam FE, Peng S, Li M, Wang J. Dynamic analysis of microbial communities and flavor properties in Merlot wines produced from inoculation and spontaneous fermentation. Food Res Int, 2023

[46]

Liu Y, Dong J, Liu G, Yang H, Liu W, Wang L, Kong C, Zheng D, Yang J, Deng L, Wang S. Co-digestion of tobacco waste with different agricultural biomass feedstocks and the inhibition of tobacco viruses by anaerobic digestion. Bioresour Technol, 2015, 189: 210-216.

[47]

Liu J, Yang C, Fan W, Xi H, Dong A, Wang D, Chai G, Mao J, Xiong G, Zong Y. Screening of seven note character impact groups in cigarette smoke. Tob Sci Technol., 2019, 52: 44-50.

[48]

Liu B, Zhao S, Li Y, He F, Yang W, Zhao M. Study on changes of carbohydrate and its related enzyme activities during drying of cigar with different maturities. J Agric Sci Technol, 2021, 23: 192-201.

[49]

Liu F, Wu Z, Zhang X, Xi G, Zhao Z, Lai M, Zhao M. Microbial community and metabolic function analysis of cigar tobacco leaves during fermentation. Microbiologyopen, 2021

[50]

Loew O (1899) Curing and fermentation of cigar leaf tobacco. US Government Printing Office, Washington, DC

[51]

Lyu C, Chen C, Ge F, Liu D, Zhao S, Chen D. A preliminary metagenomic study of puer tea during pile fermentation. J Sci Food Agric, 2013, 93: 2870.

[52]

Ma Y, Wang X, Nie X, Zhang Z, Yang Z, Nie C, Tang H. Microbial degradation of chlorogenic acid by a Sphingomonas sp Strain. Appl Biochem Biotechnol, 2016, 179: 1381-1392.

[53]

Maldonado-Robledo G, Rodriguez-Bustamante E, Sanchez-Contreras A, Rodriguez-Sanoja R, Sanchez S. Production of tobacco aroma from lutein. Specific role of the microorganisms involved in the process. Appl Microbiol Biotechnol, 2003, 62: 484-488.

[54]

Marija B, Stela J, Durđica A, Marijana B, Drago S. Carbohydrates-key players in tobacco aroma formation and quality determination. Molecules, 2020, 25: 1734.

[55]

Mathatheeranan P, Wongprasert T, Nan TN, Suwannakul E, Wang Y, Lu T, Fang M, Suppavorasatit I. Volatile profiles and aroma-active components of Northern Thai fermented soybean (thua nao) produced from controlled and uncontrolled fermentations. Int J Gastron Food S, 2023

[56]

Mckee HS. Review of recent work on nitrogen metabolism. New Phytol, 2010, 48: 1-83.

[57]

Mookherjee BD, Wilson RA (1990) Tobacco constituents—their importance in flavor and fragrance chemistry. Perfum Flavor 15:27–49

[58]

Mu Y, Chen Q, Parales RE, Lu Z, Hong Q, He J, Qiu J, Jiang J. Bacterial catabolism of nicotine: catabolic strains, pathways and modules. Environ Res, 2020

[59]

Newman MEJ. Modularity and community structure in networks. Proc Natl Acad Sci U S A, 2006, 103: 8577-8582.

[60]

Niccum BA, Kastman EK, Kfoury N, Robbat A, Wolfe BE. Strain-level diversity impacts cheese rind microbiome assembly and function. Cold Spring Harbor Lab, 2019

[61]

Ning Y, Zhang L, Mai J, Su J, Cai J, Chen Y, Jiang Y, Zhu M, Hu B. Tobacco microbial screening and application in improving the quality of tobacco in different physical states. Bioresour Bioprocess, 2023

[62]

Olesen JM, Bascompte J, Dupont YL, Jordano P. The modularity of pollination networks. Proc Natl Acad Sci U S A, 2007, 104: 19891-19896.

[63]

Peng M, Zhang X, Huang T, Zhong X, Chai L, Lu Z, Shi J, Xu Z. Komagataeibacter europaeus improves community stability and function in solid-state cereal vinegar fermentation ecosystem: non-abundant species plays important role. Food Res Int, 2021

[64]

Pineau BBJC. Which impact for β-damascenone on red wines aroma?. J Agric Food Chem, 2007

[65]

Proulx SR, Promislow D, Phillips PC. Network thinking in ecology and evolution. Trends Ecol Evol, 2005, 20: 345-353.

[66]

Ren Y, Yu G, Shi C, Liu L, Guo Q, Han C, Zhang D, Zhang L, Liu B, Gao H. Majorbio Cloud: a one-stop, comprehensive bioinformatic platform for multiomics analyses. iMeta, 2022

[67]

Salazar MMM, Lizarazo-Medina P. Assessment of the fungal community associated with cocoa bean fermentation from two regions in Colombia. Food Res Int, 2021

[68]

Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol, 2009, 75: 7537.

[69]

Shen H, Ge J, Wang Y, Shangguan M, Fang C, Guo X, Tang C. Correlation analysis of free amino acid and other major nitrogen compounds and sensory quality of flue-cured tobacco in Fujian. Acta Tabacaria Sinica, 2022, 28: 23-31.

[70]

Shendure J, Ji H. Next-generation DNA sequencing. Nat Biotechnol, 2008, 26: 1135-1145.

[71]

Shi Y, Pan Y, Du F, Zhao Z, Li Z, Wang Y, Yuan X, Zhang Z, Pang X, Wang J. Identification and discrimination of characteristic aroma components of different cigar leaves based on static headspace/gas chromatog-raphy-ion mobility spectrometry combined with relative odor activity value and multivariate statistical analysis. J Instrum Anal, 2023, 42: 674-683.

[72]

Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, Chow CT, Sachdeva R, Jones AC, Schwalbach MS, Rose JM, Hewson I, Patel A, Sun F, Caron DA, Fuhrman JA. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J, 2011, 5: 1414-1425.

[73]

Tan Y, Zhong H, Zhao D, Du H, Xu Y. Succession rate of microbial community causes flavor difference in strong-aroma Baijiu making process. Int J Food Microbiol, 2019, 311: 108350.

[74]

Tan G, Hu M, Li X, Li X, Pan Z, Li M, Li L, Wang Y, Zheng Z. Microbial community and metabolite dynamics during soy sauce koji making. Front Microbiol, 2022

[75]

Trygg J. O2-PLS for qualitative and quantitative analysis in multivariate calibration. J Chemom, 2010

[76]

Vickery HB (1950) The metabolism of the organic acids of tobacco leaves. 411–416

[77]

Wagner MR, Lundberg DS, Del Rio TG, Tringe SG, Dangl JL, Mitchell-Olds T. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat Commun, 2016

[78]

Wahlberg I, Karlsson K, Austin DJ, Junker N, Roeraade J, Enzell CR, Johnson WH. Effects of flue-curing and ageing on the volatile, neutral and acidic constituents of Virginia tobacco. Phytochemistry, 1977, 16: 1217-1231.

[79]

Wakayama M, Yamagata T, Kamemura A, Bootim N, Yano S, Tachiki T, Yoshimune K, Moriguchi M. Characterization of salt-tolerant glutaminase from Stenotrophomonas maltophilia NYW-81 and its application in Japanese soy sauce fermentation. J Ind Microbiol Biotechnol, 2005, 32: 383-390.

[80]

Wang S, Wang B, Li X, Li X. Relationship between content of free amino acids and inherent quality of flue-cured tobacco. Chinese Tob Sci, 2002, 4: 5-8.

[81]

Wang ZM, Lu ZM, Shi JS, Xu ZH. Exploring flavour-producing core microbiota in multispecies solid-state fermentation of traditional Chinese vinegar. Sci Rep, 2016, 6: 26818.

[82]

Wang F, Men X, Zhang G, Liang K, Wu L. Assessment of 16S rRNA gene primers for studying bacterial community structure and function of aging flue-cured tobaccos. AMB Express, 2018

[83]

Wang XX, Xiong HR, Wang SL, Zhang YL, Song ZH, Zhang XX. Physicochemical analysis, sensorial evaluation, astringent component identification and aroma-active compounds of herbaceous Peony (Paeonia lactiflora Pall) black tea. Ind Crops Prod, 2023

[84]

Wei X, Deng X, Cai D, Ji Z, Wang C, Yu J, Ji J, Chen S. Decreased tobacco-specific nitrosamines by microbial treatment with Bacillus amyloliquefaciens DA9 during the air-curing process of burley tobacco. J Agric Food Chem, 2014, 62: 12701-12706.

[85]

Wei F, Liu G, Yang Y, Wang F, Li Y, Guo Q. Relations between cartenoids and aromatic components from the cartenoids in flue-cured tobacco (Nicotinnatobacum L) leaves at different mature periods. Sci Agric Sinica, 2005

[86]

Wu H, Huang W, Chen Z, Chen Z, Shi J, Kong Q, Sun S, Jiang X, Chen D, Yan S. GC-MS-based metabolomic study reveals dynamic changes of chemical compositions during black tea processing. Food Res Int, 2019, 120: 330-338.

[87]

Xiang G, Yang H, Yang L, Zhang X, Cao Q, Miao M. Multivariate statistical analysis of tobacco of different origin, grade and variety according to polyphenols and organic acids. Microchem J, 2010, 95: 198-206.

[88]

Xie G, Kong X, Kang J, Su N, Fei J. Community-level dormancy potential regulates bacterial beta-diversity succession during the co-composting of manure and crop residues. Sci Total Environ, 2021, 772: 145506.

[89]

Xing L, Yang J, Jia Y, Hu X, Yi Z. Effects of ecological environment and host genotype on the phyllosphere bacterial communities of cigar tobacco (Nicotianatabacum L.). Ecol Evol, 2021

[90]

Yang H, Zhou J, Yang S, Peng Y, Zhang Y, Luo Z. Study on chiefly non-volatile organic acid of flue-cured tobacco in the different latitude producing area. J Hunan Agric University, 2005

[91]

Yang Y, Peng QY, Ou MY, Wu YX, Fang J. Research progress in tobacco fermentation. J Biosci Med, 2018

[92]

Yao L, Huang C, Ding J, Zhang T, Yu J, Yang C, Chen X. Application of yeast in plant-derived aroma formation from cigar filler leaves. Front Bioeng Biotechnol, 2022

[93]

Ye J, Zheng S, Zhang Z, Yang F, Ma K, Feng Y, Zheng J, Mao D, Yang X. Bacterial cellulose production by Acetobacter xylinum ATCC 23767 using tobacco waste extract as culture medium. Bioresour Technol, 2019, 274: 518-524.

[94]

Yuan YJ, Lu ZX, Wu N, Huang LJ, F. XL, Bie XM, . Isolation and preliminary characterization of a novel nicotine-degrading bacterium, Ochrobactrum intermedium DN2. Int Biodeterior Biodegrad, 2005, 56: 45-50.

[95]

Yue WD, Wang BY, Yu J (2023) Technology propels the realization of the "cigar" dream. Oriental Tobacco, pp.4.

[96]

Yun F, Liu G, Shi H, Yang X. Interactive effects of light intensity and nitrogen supply on the neutral volatile aroma components and organic acids of flue-cured tobacco. J Food Agric Environ, 2013, 11: 1187-1194.

[97]

Zhang G, Cao T, Ying J, Yang Y, Ma L. Diversity and novelty of actinobacteria in Arctic marine sediments. Antonie Van Leeuwenhoek, 2014, 4: 743-754.

[98]

Zang J, Xu Y, Xia W, C JMR, Yu D, Yang F, Jiang Q, . Correlations between microbiota succession and flavor formation during fermentation of Chinese low-salt fermented common carp (Cyprinuscarpio L.) inoculated with mixed starter cultures. Food Microbiol, 2020

[99]

Zang J, Yu D, Li T, Xu Y, Regenstein JM, Xia W. Identification of characteristic flavor and microorganisms related to flavor formation in fermented common carp (Cyprinuscarpio L.). Food Res Int, 2022

[100]

Zhang Z, Zhang Q, Yang H, Sun L, Xia H, Sun W, Wang Z, Zhang J. Bacterial communities related to aroma formation during spontaneous fermentation of 'Cabernet Sauvignon' wine in Ningxia. China. Foods, 2022, 11: 2775.

[101]

Zhao M, Su XQ, Nian B, Chen LJ, Ma Y. Integrated meta-omics approaches to understand the microbiome of spontaneous fermentation of traditional Chinese Pu-erh Tea. Msystems, 2019

[102]

Zhao L, Wang Y, Xing J, Gu S, Wu Y, Li X, Ma J, Mao J (2022a) Distinct succession of abundant and rare fungi in fermented grains during Chinese strong-flavor liquor fermentation. LWT-Food Sci Technol 163. https://doi.org/10.1016/j.lwt.2022.113502.

[103]

Zhao S, Wu Z, Lai M, Zhao M, Lin B (2022b) Determination of optimum humidity for air-curing of cigar tobacco leaves during the browning period. Ind Crops Prod 183. https://doi.org/10.1016/j.indcrop.2022.114939.

[104]

Zheng T, Zhang Q, Li P, Wu X, Liu Y, Yang Z, Li D, Zhang J, Du G (2022a) Analysis of microbial community, volatile flavor compounds, and flavor of cigar tobacco leaves from different regions. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.907270.

[105]

Zheng T, Zhang Q, Wu Q, Li D, Wu X, Li P, Zhou Q, Cai W, Zhang J, Du G (2022b) Effects of inoculation with Acinetobacter on fermentation of cigar tobacco leaves. Front Microbiol 13. https://doi.org/10.3389/fmicb.2022.911791.

[106]

Zhong W, Zhu C, Shu M, Sun K, Zhao L, Wang C, Ye Z, Chen J. Degradation of nicotine in tobacco waste extract by newly isolated Pseudomonas sp ZUTSKD. Bioresour Technol, 2010, 101: 6935-6941.

[107]

Zhou J, Yu L, Zhang J, Liu J, Zou X. Dynamic characteristics and co-occurrence patterns of microbial community in tobacco leaves during the 24-month aging process. Ann Microbiol, 2021

[108]

Zhu Y, Luo Y, Wang P, Zhao M, Li L, Hu X, Chen F. Simultaneous determination of free amino acids in Pu-erh tea and their changes during fermentation. Food Chem, 2016, 194: 643-649.

[109]

Zong J, He X, Lin Z, Hu M, Zou C. Effect of two drying methods on chemical transformations in flue-cured tobacco. Dry Technol, 2020

Funding

Sichuan Provincial Branch of China National Tobacco Corporation(SCYC201913)

Henan Agricultural University(3050109)

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