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Exploring the microbiota and metabolites of traditional rice beer varieties of Assam and their functionalities

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Abstract

Rice beer is traditionally prepared and consumed by various ethnic populations in the Southeast Asian countries. To understand the probable effects of rice beer on human health, present research was aimed to study biochemical parameters, microbial diversity and metabolites of major rice beer varieties of Assam, namely Apong (Poro and Nogin), Xaaj and Joubishi. Alcoholic content of rice beer varieties varied from 9.41 to 19.33% (v/v). Free radical scavenging activity against DPPH· and ABTS+ were 1.94–4.14 and 1.69–3.91 mg of ascorbic acid/ml of rice beer, respectively. In relation to antioxidant activities, phenolic content varied from 2.07 to 5.40 mg gallic acid/ml of rice beer. Next-generation sequencing of 16S rDNA showed that 18 genera of bacteria were present irrespective of rice beer varieties in which lactic acid bacteria were the dominant group (90% abundance). Functional predictions based on the bacterial profiles indicated pathways, such as metabolisms of carbohydrate, amino acid, vitamins and cofactors, and xenobiotic biodegradation, to be active in the rice beer varieties. Out of 18 core bacterial genera, 7 had correlations with the predicted functions. Gas chromatography and mass spectroscopy-based metabolite analysis revealed that the metabolite profiles of the rice beer varieties consisted of 18 saccharides, 18 organic acids, 11 sugar alcohols, 8 amino acids, 1 vitamin and nutraceutical compounds thiocoumarine, carotene, oxazolidine-2-one and acetyl tyrosine. Due to the presence of potent prebiotics, probiotics and nutraceuticals, rice beer may have health benefits which need to be studied further.

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References

  • Adak A, Maity C, Ghosh K, Halder SK, Mohapatra PKD, Mondal KC (2013) Potentialities of newly isolated Bacillus subtilis and Lactobacillus sp. for curd preparation and a comparative study of its physico-chemical parameters with other marketed curds. Indian J Exp Biol 51:910–918

    CAS  PubMed  Google Scholar 

  • Aidoo KE, Nout MJ, Sarkar PK (2006) Occurrence and function of yeasts in Asian indigenous fermented foods. FEMS Yeast Res 6:30–39. https://doi.org/10.1111/j.1567-1364.2005.00015.x

    Article  CAS  PubMed  Google Scholar 

  • Amara AA, Shibl A (2015) Role of probiotics in health improvement, infection control and disease treatment and management. Saudi Pharm J 23:107–114. https://doi.org/10.1016/j.jsps.2013.07.001

    Article  CAS  PubMed  Google Scholar 

  • Bhuyan DJ, Barooah MS, Bora SS, Singaravadivel K (2014) Biochemical and nutritional analysis of rice beer of North East India. Indian J Tradit Knowl 13:142–148

    Google Scholar 

  • Cai H, Zhang T, Zhang Q, Luo J, Cai C, Mao J (2018) Microbial diversity and chemical analysis of the starters used in traditional Chinese sweet rice wine. Food Microbiol 73:319–326

    Article  CAS  PubMed  Google Scholar 

  • Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Caputi A, Ueda M, Brown T (1968) Spectrophotometric determination of ethanol in wine. Am J Enol Vitic 19:160–165

    CAS  Google Scholar 

  • Chen RH, Chen WX, Chen HM, Zhang GF, Chen WJ (2018) Comparative evaluation of the antioxidant capacities, organic acids, and volatiles of papaya juices fermented by Lactobacillus acidophilus and Lactobacillus plantarum. J Food Qual. https://doi.org/10.1155/2018/9490435

    Article  Google Scholar 

  • Chong J, Xia J (2018) MetaboAnalystR: an R package for flexible and reproducible analysis of metabolomics data. Bioinformatics 27:4313–4314

    Article  Google Scholar 

  • Dahiya DK, Puniya M, Shandilya UK et al (2017) Gut microbiota modulation and its relationship with obesity using prebiotic fibers and probiotics: a review. Front Microbiol 8:563

    Article  PubMed  PubMed Central  Google Scholar 

  • Dangi AK, Dubey KK, Shukla P (2017) Strategies to improve Saccharomyces cerevisiae: technological advancements and evolutionary engineering. Indian J Microbiol 57:378–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das A, Deka S, Miyaji T (2012) Methodology of rice beer preparation and various plant materials used in starter culture preparation by some tribal communities of North-East India: a survey. Int Food Res J 19:101

    Google Scholar 

  • Das AJ, Khawas P, Miyaji T, Deka SC (2014) HPLC and GC-MS analyses of organic acids, carbohydrates, amino acids and volatile aromatic compounds in some varieties of rice beer from northeast India. J Inst Brew 120:244–252

    Article  CAS  Google Scholar 

  • Das G, Patra JK, Singdevsachan SK, Gouda S, Shin H-S (2016) Diversity of traditional and fermented foods of the seven sister states of India and their nutritional and nutraceutical potential: a review. Front Life Sci 9:292–312

    Article  CAS  Google Scholar 

  • Davidson PM, Taylor TM, Schmidt SE (2013) Chemical preservatives and natural antimicrobial compounds. In: Doyle MP, Buchanan RL (eds) Food microbiology. American Society of Microbiology, Washington, DC, pp 765–801

    Google Scholar 

  • Deka AK, Handique P, Deka DC (2018) Antioxidant-activity and physicochemical indices of the rice beer used by the Bodo community in North-East India. J Am Soc Brew Chem 76:112–116

    CAS  Google Scholar 

  • Doran-Peterson J, Cook DM, Brandon SK (2008) Microbial conversion of sugars from plant biomass to lactic acid or ethanol. Plant J 54(4):582–592

    Article  CAS  PubMed  Google Scholar 

  • Ghosh K, Maity C, Adak A et al (2014) Ethnic preparation of haria, a rice-based fermented beverage, in the province of lateritic West Bengal, India. Ethnobot Res Appl 12:039–049

    Google Scholar 

  • Ghosh K, Ray M, Adak A et al (2015) Microbial, saccharifying and antioxidant properties of an Indian rice based fermented beverage. Food Chem 168:196–202

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Rahaman L, Kaipeng DL, Deb D, Nath N, Tribedi P, Sharma BK (2016) Community-wise evaluation of rice beer prepared by some ethnic tribes of Tripura. J Ethn Foods 3:251–256

    Article  Google Scholar 

  • Gibson GR et al (2017) Expert consensus document: the international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14:491–502. https://doi.org/10.1038/nrgastro.2017.75

    Article  PubMed  Google Scholar 

  • Harrell FE Jr, Harrell MFE Jr (2018) Package ‘Hmisc’ R foundation for statistical computing. http://biostat.mc.vanderbilt.edu/Hmisc

  • Hostettmann K, Borloz A, Urbain A, Marston A (2006) Natural product inhibitors of acetylcholinesterase. Curr Org Chem 10:825–847

    Article  CAS  Google Scholar 

  • Huang ZR, Guo WL, Zhou WB et al (2018) Microbial communities and volatile metabolites in different traditional fermentation starters used for Hong Qu glutinous rice wine. Food Res Int. https://doi.org/10.1016/j.foodres.2018.12.024

    Article  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Furumichi M et al (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38:D355–D360

    Article  CAS  PubMed  Google Scholar 

  • Karnovsky A et al (2011) Metscape 2 bioinformatics tool for the analysis and visualization of metabolomics and gene expression data. Bioinformatics 28:373–380

    Article  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan MR, Bhaskar B, Adak A, Talukdar NC (2017) Rice based beverage with high alcohol content and method therefor (Application No. 201731006470, Publication Date: 17/03/2017)

  • Langille MGI et al (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814. https://doi.org/10.1038/nbt.2676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langstaff SA, Lewis MJ (1993) The mouthfeel of beer—a review. J Inst Brewing 99:31–37

    Article  CAS  Google Scholar 

  • Mäkinen KK (2016) Gastrointestinal disturbances associated with the consumption of sugar alcohols with special consideration of Xylitol: scientific review and instructions for dentists and other health-care professionals. Int J Dent Res 2016:1–16

    Google Scholar 

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. https://doi.org/10.1371/journal.pone.0009490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quast C et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219

    Article  CAS  PubMed  Google Scholar 

  • Ray M, Ghosh K, Singh S, Mondal KC (2016) Folk to functional: an explorative overview of rice-based fermented foods and beverages in India. J Ethn Foods 3:5–18

    Article  Google Scholar 

  • Rognes T, Flouri T, Nichols B et al (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584

    Article  PubMed  PubMed Central  Google Scholar 

  • Romi W, Ahmed G, Jeyaram K (2015) Three-phase succession of autochthonous lactic acid bacteria to reach a stable ecosystem within 7 days of natural bamboo shoot fermentation as revealed by different molecular approaches. Mol Ecol 24:3372–3389

    Article  PubMed  Google Scholar 

  • Sha SP, Jani K, Sharma A et al (2017) Analysis of bacterial and fungal communities in Marcha and Thiat, traditionally prepared amylolytic starters of India. Sci Rep 7:10967

    Article  PubMed  PubMed Central  Google Scholar 

  • Shannon P et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shewry PR, Hey SJ (2015) The contribution of wheat to human diet and health. Food Energy Secur 4:178–202. https://doi.org/10.1002/fes3.64

    Article  PubMed  PubMed Central  Google Scholar 

  • Shukla S, Shukla A, Mehboob S et al (2011) Meta-analysis: the effects of gut flora modulation using prebiotics, probiotics and synbiotics on minimal hepatic encephalopathy. Aliment Pharmacol Ther 33:662–671

    Article  CAS  PubMed  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. In: Packer L (ed) Methods in enzymology, vol 299. Academic Press, Cambridge, pp 152–178. https://doi.org/10.1016/S0076-6879(99)99017-1

    Chapter  Google Scholar 

  • Sokrab AM, Mohamed Ahmed IA, Babiker EE (2014) Effect of fermentation on antinutrients, and total and extractable minerals of high and low phytate corn genotypes. J Food Sci Technol 51:2608–2615. https://doi.org/10.1007/s13197-012-0787-8

    Article  CAS  PubMed  Google Scholar 

  • Steinkraus KH (1983) Effect of pre and post fermentation treatments on quality of red wine preparation from punjab purple grapes. Antonie van Leeuwenhoek 49:12

    Article  Google Scholar 

  • Tanaka S, Yamamoto K, Yamada K et al (2016) Relationship of enhanced butyrate production by colonic butyrate-producing bacteria to immunomodulatory effects in normal mice fed an insoluble fraction of Brassica rapa L. Appl Environ Microbiol 82:2693–2699. https://doi.org/10.1128/AEM.03343-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vandenbergh PA (1993) Lactic acid bacteria, their metabolic products and interference with microbial growth. FEMS Microbiol Rev 12:221–237

    Article  CAS  Google Scholar 

  • Warnes GR et al (2009) gplots: Various R programming tools for plotting data R package version 2:1

  • Wei T, Simko V, Levy M et al (2017) Package ‘corrplot’. Statistician 56:316–324

    Google Scholar 

  • Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer

  • Wookey A, Turner PJ, Greenhalgh JM, Eastwood M, Clarke J, Sefton C (2004) AZD2563, a novel oxazolidinone: definition of antibacterial spectrum, assessment of bactericidal potential and the impact of miscellaneous factors on activity in vitro. Clin Microbiol Infect 10:247–254. https://doi.org/10.1111/j.1198-743X.2004.00770.x

    Article  CAS  PubMed  Google Scholar 

  • Yadav R, Shukla P (2017) Probiotics for human health: current progress and applications. In: Shukla P (ed) Recent advances in applied microbiology. Springer, Singapore, pp 133–147

    Chapter  Google Scholar 

  • Yadav R, Puniya AK, Shukla P (2016) Probiotic properties of Lactobacillus plantarum RYPR1 from an indigenous fermented beverage Raabadi. Front Microbiol 7:1683

    PubMed  PubMed Central  Google Scholar 

  • Yamazaki A, Li J, Hutchins WC et al (2011) Commensal effect of pectate lyases secreted from Dickeya dadantii on proliferation of Escherichia coli O157:H7 EDL933 on lettuce leaves. Appl Environ Microbiol 77:156–162. https://doi.org/10.1128/AEM.01079-10

    Article  CAS  PubMed  Google Scholar 

  • Zapata PJ, Martínez-Esplá A, Gironés-Vilaplana A et al (2019) Phenolic, volatile, and sensory profiles of beer enriched by macerating quince fruits. LWT 103:139–146

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the Institutional level Biotech Hub (DBT, Govt. of India) and Central instrumentation facility of IASST for providing the facilities. This research was funded by Department of Biotechnology (DBT) under the Unit of Excellence Project (BT/550/NE/U-Excel/2014). The authors would like to thank Mr. Anupam Bhattacharya, Research Associate, BIF centre IASST for assistance in computational analysis. The authors are also thankful to volunteers for providing samples.

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Das, S., Deb, D., Adak, A. et al. Exploring the microbiota and metabolites of traditional rice beer varieties of Assam and their functionalities. 3 Biotech 9, 174 (2019). https://doi.org/10.1007/s13205-019-1702-z

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