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References

  1. Kim YH, An YJ. 2020. Development of a standardized new cigarette smoke generating (SNCSG) system for the assessment of chemicals in the smoke of new cigarette types (heat-not-burn (HNB) tobacco and electronic cigarettes (E-Cigs)). Environ. Res. 185: 109413.
  2. Simonavicius E, McNeill A, Shahab L, Brose LS. 2019. Heat-not-burn tobacco products: a systematic literature review. Tob. Control 28: 582-594.
  3. Li X, Luo Y, Jiang X, Zhang H, Zhu F, Hu S, et al. 2019. Chemical analysis and simulated pyrolysis of tobacco heating system 2.2 compared to conventional cigarettes. Nicotine Tob. Res. 21: 111-118.
  4. Farsalinos KE, Yannovits N, Sarri T, Voudris V, Poulas K. 2018. Nicotine delivery to the aerosol of a heat-not-burn tobacco product:comparison with a tobacco cigarette and E-cigarettes. Nicotine Tob. Res. 20: 1004-1009.
  5. Znyk M, Jurewicz J, Kaleta D. 2021. Exposure to heated tobacco products and adverse health effects, a systematic review. Int. J. Environ. Res. Public Health 18: 6651.
  6. Ning Y, Mai J, Hu BB, Lin ZL, Chen Y, Jiang YL, et al. 2023. Study on the effect of enzymatic treatment of tobacco on HnB cigarettes and microbial succession during fermentation. Appl. Microbiol. Biotechnol. 107: 4217-4232.
  7. Popova V, Ivanova T, Prokopov T, Nikolova M, Stoyanova A, Zheljazkov VD. 2019. Carotenoid-related volatile compounds of tobacco (Nicotiana tabacum L.) essential oils. Molecules 24: 3446.
  8. Yin F, Karangwa E, Song S, Duhoranimana E, Lin S, Cui H, et al. 2019. Contribution of tobacco composition compounds to characteristic aroma of Chinese faint-scent cigarettes through chromatography analysis and partial least squares regression. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1105: 217-227.
  9. Weeks WW, Sisson VA, Chaplin JF. 1992. Differences in aroma, chemistry, solubilities, and smoking quality of cured flue-cured tobaccos with aglandular and glandular trichomes. J. Agric. Food Chem. 40: 1911-1916.
  10. Zheng T, Zhang Q, Li P, Wu X, Liu Y, Yang Z, et al. 2022. Analysis of microbial community, volatile flavor compounds, and flavor of cigar tobacco leaves from different regions. Front. Microbiol. 13: 907270.
  11. Liu F, Zhao Z, Zhao M. 2016. Detection and quantitative analysis of dominant bacteria on aging flue-cured tobacco leaves. Agric. Sci. Technol. 17: 2611-2614.
  12. Wen C, Zhang Q, Zhu P, Hu W, Jia Y, Yang S, et al. 2023. High throughput screening of key functional strains based on improving tobacco quality and mixed fermentation. Front. Bioeng. Biotechnol. 11: 1108766.
  13. Hu B, Gu K, Gong J, Zhang K, Chen D, He X, et al. 2021. The effect of flue-curing procedure on the dynamic change of microbial diversity of tobaccos. Sci. Rep. 11: 5354.
  14. Zhang Q, Kong G, Zhao G, Liu J, Jin H, Li Z, et al. 2023. Microbial and enzymatic changes in cigar tobacco leaves during air-curing and fermentation. Appl. Microbiol. Biotechnol. 107: 5789-5801.
  15. Liu F, Wu Z, Zhang X, Xi G, Zhao Z, Lai M, et al. 2021. Microbial community and metabolic function analysis of cigar tobacco leaves during fermentation. Microbiologyopen 10: e1171.
  16. Banožić M, Jokić S, Ačkar Đ, Blažić M, Šubarić D. 2020. Carbohydrates-key players in tobacco aroma formation and quality determination. Molecules 25: 1734.
  17. Liu T, Guo S, Wu C, Zhang R, Zhong Q, Shi H, et al. 2022. Phyllosphere microbial community of cigar tobacco and its corresponding metabolites. Front. Microbiol. 13: 1025881.
  18. Zheng T, Zhang Q, Wu Q, Li D, Wu X, Li P, et al. 2022. Effects of inoculation with acinetobacter on fermentation of cigar tobacco leaves. Front. Microbiol. 13: 911791.
  19. Xu Q, Li S, Huang S, Mao D. 2021. Review on tobacco-derived microorganisms and its application. J. Light Ind. 36: 42-50+58.
  20. Zheng Z. 2021. Study on the microbial diversity of tobacco and its effect on the fermentation quality of tobacco. Master. Northwest A&F University.
  21. Ma L, Wang Y, Wang X, Lü X. 2023. Solid-state fermentation improves tobacco leaves quality via the screened Bacillus subtilis of simultaneously degrading starch and protein ability. Appl. Biochem. Biotechnol. 196: 506-521.
  22. Dai J, Dong A, Xiong G, Liu Y, Hossain MS, Liu S, et al. 2020. 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. 11: 1539.
  23. Li J, Zhao Y, Qin Y, Shi H. 2020. Influence of microbiota and metabolites on the quality of tobacco during fermentation. BMC Microbiol. 20: 356.
  24. Zhou J, Yu L, Zhang J, Zhang X, Xue Y, Liu J, et al. 2020. Characterization of the core microbiome in tobacco leaves during aging. Microbiologyopen 9: e984.
  25. Ren M, Qin Y, Zhang L, Zhao Y, Zhang R, Shi H. 2023. Effects of fermentation chamber temperature on microbes and quality of cigar wrapper tobacco leaves. Appl. Microbiol. Biotechnol. 107: 6469-6485.
  26. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
  27. Huang J, Yang J, Duan Y, Gu W, Gong X, Zhe W, et al. 2010. Bacterial diversities on unaged and aging flue-cured tobacco leaves estimated by 16S rRNA sequence analysis. Appl. Microbiol. Biotechnol. 88: 553-562.
  28. Liu F, Zhang X, Wang M, Guo L, Yang Y, Zhao M. 2020. Biosorption of sterols from tobacco waste extract using living and dead of newly isolated fungus Aspergillus fumigatus strain LSD-1. Biosci. Biotechnol. Biochem. 84: 1521-1528.
  29. Gong Y, Li J, Deng X, Chen Y, Chen S, Huang H, et al. 2023. Application of starch degrading bacteria from tobacco leaves in improving the flavor of flue-cured tobacco. Front. Microbiol. 14: 1211936.
  30. Ye J, Zhang Z, Yan J, Hao H, Liu X, Yang Z, et al. 2017. Degradation of phytosterols in tobacco waste extract by a novel Paenibacillus sp. Biotechnol. Appl. Biochem. 64: 843-850.
  31. Carpenter CM, Wayne GF, Connolly GN. 2007. The role of sensory perception in the development and targeting of tobacco products. Addiction 102: 136-147.
  32. Zong P, Hu W, Huang Y, An H, Zhang Q, Chai Z, et al. 2023. Effects of adding cocoa fermentation medium on cigar leaves in agricultural fermentation stage. Front. Bioeng. Biotechnol. 11: 1251413.
  33. Liu H, Hu L, Yan K, Long M, Shan X, Zi W. 2015. Study on changes in. internal chemical components of flue-cured tobacco in process of natural alcoholization. Acta Agric. Jiangxi. 27: 71-75.
  34. Hu W, Cai W, Zheng Z, Liu Y, Luo C, Xue F, et al. 2022. Study on the. chemical compositions and microbial communities of cigar tobacco leaves fermented with exogenous additive. Sci. Rep. 12: 19182.
  35. Zhou G, Chen J, Kong L, Yang S, Xia Q, Liu J, et al. 2014. Analysis of aroma components of diverse tobacco materials in main tobacco areas of Yunnan. Southwest China J. Agric. Sci . 27: 1058-1061.
  36. Ding Y, Zhu L, Liu S, Yu H, Dai Y. 2013. Analytical method of free and conjugated neutral aroma components in tobacco by solvent extraction coupled with comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry. J. Chromatogr. A. 1280: 122-127.
  37. Zhang Q, Ma Z, Meng Q, Li D, Ding Z. 2021. Key aroma compounds and metabolic profiling of Debaryomyces hansenii L1-1fermented flos sophorae. J. Food Biochem. 45: e13711.
  38. Landis EA, Fogarty E, Edwards JC, Popa O, Eren AM, Wolfe BE. 2022. Microbial diversity and interaction specificity in Kombucha tea fermentations. mSystems 7: e0015722.
  39. Tang Q, Liu T, Teng K, Xiao Z, Cai H, Wang Y, et al. 2023. Microbial interactions and metabolisms in response to bacterial wilt and black shank pathogens in the tobacco rhizosphere. Front. Plant Sci. 14: 1200136.
  40. Zhou M, Sun C, Dai B, He Y, Zhong J. 2023. Intercropping system modulated soil-microbe interactions that enhanced the growth and quality of flue-cured tobacco by improving rhizospheric soil nutrients, microbial structure, and enzymatic activities. Front. Plant Sci. 14: 1233464.
  41. Gao J, Uwiringiyimana E, Zhang D. 2023. Microbial composition and diversity of the tobacco leaf phyllosphere during plant development. Front. Microbiol. 14: 1199241.
  42. Zhang G, Zhao L, Li W, Yao H, Lu C, Zhao G, et al. 2023. Changes in physicochemical properties and microbial community succession during leaf stacking fermentation. AMB Express 13: 132.
  43. Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, Kuhlemeier C. 2002. The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J. 30: 329-336.
  44. Pan D, Sun M, Wang Y, Lv P, Wu X, Li QX, et al. 2018. Characterization of nicotine catabolism through a novel pyrrolidine pathway in Pseudomonas sp. S-1. J. Agric. Food Chem. 66: 7393-7401.
  45. Li J, Yi F, Chen G, Pan F, Yang Y, Shu M, et al. 2021. Function enhancement of a metabolic module via endogenous promoter replacement for Pseudomonas sp. JY-Q to degrade nicotine in tobacco waste treatment. Appl. Biochem. Biotechnol. 193: 2793-2805.

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Article

Research article

J. Microbiol. Biotechnol. 2024; 34(9): 1890-1897

Published online September 28, 2024 https://doi.org/10.4014/jmb.2402.02039

Copyright © The Korean Society for Microbiology and Biotechnology.

Analyzing the Effect of Microbial Consortia Fermentation on the Quality of HnB by Untargeted Metabolomics

Ling Zou1,2, Hong Zhang3, Zhonghua Liu3, Jianfeng Sun3, Yang Hu4, Yishu Ding4, Xinwei Ji5, Zhenfei Yang5, Qi Zhang2*, and Binbin Hu1*

1Yunnan Academy of Tobacco Agricultural Science, Kunming 650021, Yunnan, P.R. China
2Faculty of Life Science and Technology, Kunming University of Science and Technology, Kunming 650500, Yunnan, P.R. China
3China National Tobacco Corporation Yunnan Company, Kunming 650032, P.R. China
4Chuxiong Prefecture Branch of Yunnan Tobacco Company, Chuxiong 675000, P.R. China
5Honghe Prefecture Branch of Yunnan Tobacco Company, Honghe, P.R. China

Correspondence to:Qi Zhang,        qzhang37@kust.edu.cn
Binbin Hu,        hubinbin20072008@163.com

Received: February 23, 2024; Revised: June 6, 2024; Accepted: July 2, 2024

Abstract

Fermentation has been identified as an effective strategy to alter the chemical makeup of tobacco, thereby enhancing its quality. The deliberate introduction of microorganisms can hasten the fermentation process. In this research, microbial consortia harvested from the tobacco surface were utilized to enhance the tobacco quality. This enhancement also elevated several sensory attributes of HnB cigarettes, such as aroma richness, moisture, strength, and reduced irritation, achieving a sensory quality rating of 84.5. This marks a notable improvement compared to the 82 rating of the original, unfermented cigarettes. Untargeted metabolomics analysis revealed a decrease in total polyphenols and unsaturated fatty acids, while the levels of polyacids, alcohols, ketones, furans, and other compounds increased in the fermented tobacco. Additionally, KEGG pathway enrichment analysis indicated that the enhancement in tobacco quality through microbial consortia fermentation is linked to various biological pathways, with pathways related to fatty acid and amino acid degradation playing pivotal roles. The findings of this study will serve as a reference for the commercial production of HnB cigarettes, and the elucidated mechanism offers a theoretical basis for exploring microbial fermentation as a means to improve tobacco quality.

Keywords: Microbial consortia, fermentation, HnB cigarettes, metabolomics, mechanisms

References

  1. Kim YH, An YJ. 2020. Development of a standardized new cigarette smoke generating (SNCSG) system for the assessment of chemicals in the smoke of new cigarette types (heat-not-burn (HNB) tobacco and electronic cigarettes (E-Cigs)). Environ. Res. 185: 109413.
  2. Simonavicius E, McNeill A, Shahab L, Brose LS. 2019. Heat-not-burn tobacco products: a systematic literature review. Tob. Control 28: 582-594.
  3. Li X, Luo Y, Jiang X, Zhang H, Zhu F, Hu S, et al. 2019. Chemical analysis and simulated pyrolysis of tobacco heating system 2.2 compared to conventional cigarettes. Nicotine Tob. Res. 21: 111-118.
  4. Farsalinos KE, Yannovits N, Sarri T, Voudris V, Poulas K. 2018. Nicotine delivery to the aerosol of a heat-not-burn tobacco product:comparison with a tobacco cigarette and E-cigarettes. Nicotine Tob. Res. 20: 1004-1009.
  5. Znyk M, Jurewicz J, Kaleta D. 2021. Exposure to heated tobacco products and adverse health effects, a systematic review. Int. J. Environ. Res. Public Health 18: 6651.
  6. Ning Y, Mai J, Hu BB, Lin ZL, Chen Y, Jiang YL, et al. 2023. Study on the effect of enzymatic treatment of tobacco on HnB cigarettes and microbial succession during fermentation. Appl. Microbiol. Biotechnol. 107: 4217-4232.
  7. Popova V, Ivanova T, Prokopov T, Nikolova M, Stoyanova A, Zheljazkov VD. 2019. Carotenoid-related volatile compounds of tobacco (Nicotiana tabacum L.) essential oils. Molecules 24: 3446.
  8. Yin F, Karangwa E, Song S, Duhoranimana E, Lin S, Cui H, et al. 2019. Contribution of tobacco composition compounds to characteristic aroma of Chinese faint-scent cigarettes through chromatography analysis and partial least squares regression. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 1105: 217-227.
  9. Weeks WW, Sisson VA, Chaplin JF. 1992. Differences in aroma, chemistry, solubilities, and smoking quality of cured flue-cured tobaccos with aglandular and glandular trichomes. J. Agric. Food Chem. 40: 1911-1916.
  10. Zheng T, Zhang Q, Li P, Wu X, Liu Y, Yang Z, et al. 2022. Analysis of microbial community, volatile flavor compounds, and flavor of cigar tobacco leaves from different regions. Front. Microbiol. 13: 907270.
  11. Liu F, Zhao Z, Zhao M. 2016. Detection and quantitative analysis of dominant bacteria on aging flue-cured tobacco leaves. Agric. Sci. Technol. 17: 2611-2614.
  12. Wen C, Zhang Q, Zhu P, Hu W, Jia Y, Yang S, et al. 2023. High throughput screening of key functional strains based on improving tobacco quality and mixed fermentation. Front. Bioeng. Biotechnol. 11: 1108766.
  13. Hu B, Gu K, Gong J, Zhang K, Chen D, He X, et al. 2021. The effect of flue-curing procedure on the dynamic change of microbial diversity of tobaccos. Sci. Rep. 11: 5354.
  14. Zhang Q, Kong G, Zhao G, Liu J, Jin H, Li Z, et al. 2023. Microbial and enzymatic changes in cigar tobacco leaves during air-curing and fermentation. Appl. Microbiol. Biotechnol. 107: 5789-5801.
  15. Liu F, Wu Z, Zhang X, Xi G, Zhao Z, Lai M, et al. 2021. Microbial community and metabolic function analysis of cigar tobacco leaves during fermentation. Microbiologyopen 10: e1171.
  16. Banožić M, Jokić S, Ačkar Đ, Blažić M, Šubarić D. 2020. Carbohydrates-key players in tobacco aroma formation and quality determination. Molecules 25: 1734.
  17. Liu T, Guo S, Wu C, Zhang R, Zhong Q, Shi H, et al. 2022. Phyllosphere microbial community of cigar tobacco and its corresponding metabolites. Front. Microbiol. 13: 1025881.
  18. Zheng T, Zhang Q, Wu Q, Li D, Wu X, Li P, et al. 2022. Effects of inoculation with acinetobacter on fermentation of cigar tobacco leaves. Front. Microbiol. 13: 911791.
  19. Xu Q, Li S, Huang S, Mao D. 2021. Review on tobacco-derived microorganisms and its application. J. Light Ind. 36: 42-50+58.
  20. Zheng Z. 2021. Study on the microbial diversity of tobacco and its effect on the fermentation quality of tobacco. Master. Northwest A&F University.
  21. Ma L, Wang Y, Wang X, Lü X. 2023. Solid-state fermentation improves tobacco leaves quality via the screened Bacillus subtilis of simultaneously degrading starch and protein ability. Appl. Biochem. Biotechnol. 196: 506-521.
  22. Dai J, Dong A, Xiong G, Liu Y, Hossain MS, Liu S, et al. 2020. 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. 11: 1539.
  23. Li J, Zhao Y, Qin Y, Shi H. 2020. Influence of microbiota and metabolites on the quality of tobacco during fermentation. BMC Microbiol. 20: 356.
  24. Zhou J, Yu L, Zhang J, Zhang X, Xue Y, Liu J, et al. 2020. Characterization of the core microbiome in tobacco leaves during aging. Microbiologyopen 9: e984.
  25. Ren M, Qin Y, Zhang L, Zhao Y, Zhang R, Shi H. 2023. Effects of fermentation chamber temperature on microbes and quality of cigar wrapper tobacco leaves. Appl. Microbiol. Biotechnol. 107: 6469-6485.
  26. Edgar RC. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10: 996-998.
  27. Huang J, Yang J, Duan Y, Gu W, Gong X, Zhe W, et al. 2010. Bacterial diversities on unaged and aging flue-cured tobacco leaves estimated by 16S rRNA sequence analysis. Appl. Microbiol. Biotechnol. 88: 553-562.
  28. Liu F, Zhang X, Wang M, Guo L, Yang Y, Zhao M. 2020. Biosorption of sterols from tobacco waste extract using living and dead of newly isolated fungus Aspergillus fumigatus strain LSD-1. Biosci. Biotechnol. Biochem. 84: 1521-1528.
  29. Gong Y, Li J, Deng X, Chen Y, Chen S, Huang H, et al. 2023. Application of starch degrading bacteria from tobacco leaves in improving the flavor of flue-cured tobacco. Front. Microbiol. 14: 1211936.
  30. Ye J, Zhang Z, Yan J, Hao H, Liu X, Yang Z, et al. 2017. Degradation of phytosterols in tobacco waste extract by a novel Paenibacillus sp. Biotechnol. Appl. Biochem. 64: 843-850.
  31. Carpenter CM, Wayne GF, Connolly GN. 2007. The role of sensory perception in the development and targeting of tobacco products. Addiction 102: 136-147.
  32. Zong P, Hu W, Huang Y, An H, Zhang Q, Chai Z, et al. 2023. Effects of adding cocoa fermentation medium on cigar leaves in agricultural fermentation stage. Front. Bioeng. Biotechnol. 11: 1251413.
  33. Liu H, Hu L, Yan K, Long M, Shan X, Zi W. 2015. Study on changes in. internal chemical components of flue-cured tobacco in process of natural alcoholization. Acta Agric. Jiangxi. 27: 71-75.
  34. Hu W, Cai W, Zheng Z, Liu Y, Luo C, Xue F, et al. 2022. Study on the. chemical compositions and microbial communities of cigar tobacco leaves fermented with exogenous additive. Sci. Rep. 12: 19182.
  35. Zhou G, Chen J, Kong L, Yang S, Xia Q, Liu J, et al. 2014. Analysis of aroma components of diverse tobacco materials in main tobacco areas of Yunnan. Southwest China J. Agric. Sci . 27: 1058-1061.
  36. Ding Y, Zhu L, Liu S, Yu H, Dai Y. 2013. Analytical method of free and conjugated neutral aroma components in tobacco by solvent extraction coupled with comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry. J. Chromatogr. A. 1280: 122-127.
  37. Zhang Q, Ma Z, Meng Q, Li D, Ding Z. 2021. Key aroma compounds and metabolic profiling of Debaryomyces hansenii L1-1fermented flos sophorae. J. Food Biochem. 45: e13711.
  38. Landis EA, Fogarty E, Edwards JC, Popa O, Eren AM, Wolfe BE. 2022. Microbial diversity and interaction specificity in Kombucha tea fermentations. mSystems 7: e0015722.
  39. Tang Q, Liu T, Teng K, Xiao Z, Cai H, Wang Y, et al. 2023. Microbial interactions and metabolisms in response to bacterial wilt and black shank pathogens in the tobacco rhizosphere. Front. Plant Sci. 14: 1200136.
  40. Zhou M, Sun C, Dai B, He Y, Zhong J. 2023. Intercropping system modulated soil-microbe interactions that enhanced the growth and quality of flue-cured tobacco by improving rhizospheric soil nutrients, microbial structure, and enzymatic activities. Front. Plant Sci. 14: 1233464.
  41. Gao J, Uwiringiyimana E, Zhang D. 2023. Microbial composition and diversity of the tobacco leaf phyllosphere during plant development. Front. Microbiol. 14: 1199241.
  42. Zhang G, Zhao L, Li W, Yao H, Lu C, Zhao G, et al. 2023. Changes in physicochemical properties and microbial community succession during leaf stacking fermentation. AMB Express 13: 132.
  43. Mellema S, Eichenberger W, Rawyler A, Suter M, Tadege M, Kuhlemeier C. 2002. The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J. 30: 329-336.
  44. Pan D, Sun M, Wang Y, Lv P, Wu X, Li QX, et al. 2018. Characterization of nicotine catabolism through a novel pyrrolidine pathway in Pseudomonas sp. S-1. J. Agric. Food Chem. 66: 7393-7401.
  45. Li J, Yi F, Chen G, Pan F, Yang Y, Shu M, et al. 2021. Function enhancement of a metabolic module via endogenous promoter replacement for Pseudomonas sp. JY-Q to degrade nicotine in tobacco waste treatment. Appl. Biochem. Biotechnol. 193: 2793-2805.