Lactic acid bacteria diversity and dynamics in Colombian coffee fermentation

Authors

  • Rosmery Cruz O'Byrne Universidad del Magdalena, Facultad de Ingeniería, Grupo de Investigación Suelo, Ambiente y Sociedad/GISAS. Santa Marta, Colombia. https://orcid.org/0000-0003-3781-0771
  • Nelson Piraneque-Gambasica Universidad del Magdalena, Facultad de Ingeniería, Grupo de Investigación Suelo, Ambiente y Sociedad/GISAS. Santa Marta, Colombia. https://orcid.org/0000-0002-4264-9428
  • Sonia Aguirre-Forero Universidad del Magdalena, Facultad de Ingeniería, Grupo de Investigación Suelo, Ambiente y Sociedad/GISAS. Santa Marta, Colombia. https://orcid.org/0000-0002-6975-1940

DOI:

https://doi.org/10.25186/.v18i.2141

Abstract

Lactic acid bacteria (LAB) are recognized in coffee fermentation as key microorganisms in forming flavor and aroma precursors associated with high-quality beverages. In Colombia, although coffees with differential sensory characteristics are produced from one region to another, only some studies have been performed on the microbiology of coffee fermentation, of which no research focused on LAB species has been reported. In this study, LAB diversity and dynamics associated with coffee fermentation in the Sierra Nevada de Santa Marta (SNSM) were determined through a temporal high-throughput sequencing approach, where the 16S rRNA gene was amplified and sequenced using the Illumina MiSeq platform. Finally, LAB species were identified using the BLASTN algorithms of the NCBI GenBank. The coffee fermentation process that lasted 36 hours was dominated by the genera Leuconostoc, followed by Lactobacillus and Weissella. Of the 118 OTUs corresponding to LAB, it was possible to identify 50 bacterial species, among which 28 are reported for the first time in coffee fermentation. Among the species widely reported in coffee fermentation are Leuconostoc mesenteroides, Leuconostoc pseudomesenteroides, Lactiplantibacillus plantarum (basonym: Lactobacillus plantarum), Levilactobacillus brevis (basonym: Lactobacillus brevis), and Lactococcus lactis. While the novel reports mainly correspond to species belonging to genera that were previously recognized as Lactobacillus, such as Lactiplantibacillus, Paucilactobacillus, Secundilactobacillus, Liquorilactobacillus, Lacticaseibacillus, Schleiferilactobacillus, Loigolactobacillus, Ligilactobacillus, Lentilactobacillus, Limosilactobacillus, and Latilactobacillus. These findings suggest that the indigenous LAB of the SNSM are responsible for generating metabolites that develop specific characteristics of coffee in the region, which is why coffee from the SNSM is protected by designation of origin. Isolates of the reported species should be considered for application as starter cultures.

Key words: LAB; Lactobacillus; Leuconostoc; sequencing; Weissella.

References

AVALLONE, S. et al. Microbiological and biochemical study of coffee fermentation. Current Microbiology, 42(4):252-256, 2001.

BRAGA, A. V. U. et al. Study on coffee quality improvement by self-induced anaerobic fermentation: Microbial diversity and enzymatic activity. Food Research International, 165:112528, 2023.

CAPORASO, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6:1621-1624, 2012.

CARVALHO FERREIRA, L. et al. Coffee fermentation process: A review. Food Research International, 169:112793, 2023.

CASSIMIRO, D. M. de. J. et al. Coinoculation of lactic acid bacteria and yeasts increases the quality of wet fermented arabica coffee. International Journal of Food Microbiology, 369:109627, 2022.

CERNY, C. et al. Furfuryl alcohol is a precursor for furfurylthiol in coffee. Food Chemistry, 337:128008, 2021.

COLE, J. R. et al. Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Research, 42(D1):D633-D642, 2014.

CRUZ-O’BYRNE, R.; PIRANEQUE-GAMBASICA, N.; AGUIRRE-FORERO, S. Microbial diversity associated with spontaneous coffee bean fermentation process and specialty coffee production in northern Colombia. International Journal of Food Microbiology, 354:109282, 2021.

DE BRUYN, F. et al. Exploring the impacts of postharvest processing on the microbiota and metabolite profiles during green coffee bean production. Applied and Environmental Microbiology, 83:e02398-16, 2016.

DE BRUYNE, K. et al. Leuconostoc holzapfelii sp. nov., isolated from Ethiopian coffee fermentation and assessment of sequence analysis of housekeeping genes for delineation of Leuconostoc species. International Journal of Systematic and Evolutionary Microbiology, 57(12):2952-2959, 2007.

DE CARVALHO NETO, D. P. et al. Efficient coffee beans mucilage layer removal using lactic acid fermentation in a stirred-tank bioreactor: Kinetic, metabolic and sensorial studies. Food Bioscience, 26:80-87, 2018.

DE MELO PEREIRA, G. V. et al. Lactic acid bacteria: What coffee industry should know? Current Opinion in Food Science, 31:1-8, 2020.

DE MELO PEREIRA, G. V. et al. Potential of lactic acid bacteria to improve the fermentation and quality of coffee during on-farm processing. International Journal of Food Science & Technology, 51(7):1689-1695, 2016.

DE OLIVEIRA JUNQUEIRA, A. C. et al. First description of bacterial and fungal communities in Colombian coffee beans fermentation analysed using Illumina-based amplicon sequencing. Scientific Reports, 9:8794, 2019.

DE OLIVEIRA JUNQUEIRA, A. C. et al. Isolation and selection of fructose-consuming lactic acid bacteria associated with coffee bean fermentation. Food Biotechnology, 36: 58-75, 2022.

EDWARDS, C. G. et al. Lactobacillus nagelii sp. nov., an organism isolated from a partially fermented wine. International Journal of Systematic and Evolutionary Microbiology, 50(2):699-702, 2000.

ELHALIS, H.; COX, J.; ZHAO, J. Coffee fermentation: Expedition from traditional to controlled process and perspectives for industrialization. Applied Food Research, 3:100253, 2023.

ELHALIS, H.; COX, J.; ZHAO, J. Ecological diversity, evolution and metabolism of microbial communities in the wet fermentation of Australian coffee beans. International Journal of Food Microbiology, 321:108544, 2020.

EVANGELISTA, S. R. et al. Microbiological diversity associated with the spontaneous wet method of coffee fermentation. International Journal of Food Microbiology, 210:102-112, 2015.

FEINER, G. The microbiology of specific bacteria. In: FEINER, G. Meat products handbook: Practical science and technology. Cambridge, United Kingdom: Woodhead Publishing, p.595-615, 2006.

FENG, X. et al. Culture-dependent and independent methods to investigate the predominant microorganisms associated with wet processed coffee. Current Microbiology, 73:190-195, 2016.

FORTINA, M. G. et al. Molecular analysis of artisanal Italian cheeses reveals Enterococcus italicus sp. nov. International Journal of Systematic and Evolutionary Microbiology, 54(5):1717-1721, 2004.

GROSCH, W. et al. Sensory studies on the key odorants of roasted coffee. In: PARLIMENT, T. H.; HO, C.; SCHIEBERLE, P. Caffeinated beverages: Health benefits, physiological effects, and chemistry. Washington, United States: American Chemical Society, p. 202-209, 2000.

GU, C. T. et al. Lactobacillus mudanjiangensis sp. nov., Lactobacillus songhuajiangensis sp. nov. and Lactobacillus nenjiangensis sp. nov., isolated from Chinese traditional pickle and sourdough. International Journal of Systematic and Evolutionary Microbiology, 63(Pt_12):4698-4706, 2013.

HAMDOUCHE, Y. et al. Discrimination of post-harvest coffee processing methods by microbial ecology analyses. Food Control, 65:112-120, 2016.

HERLEMANN, D. P. et al. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal, 5(10):1571-1579, 2011.

HUCH, M.; FRANZ, C. M. A. P. Coffee: Fermentation and microbiota. In: HOLZAPFEL, W. Advances in fermented foods and beverages: improving quality, technologies and health benefits. Cambridge, United Kingdom: Woodhead Publishing, p.501-513, 2015.

ILLUMINA. 16S metagenomic sequencing library preparation: Preparing 16S ribosomal RNA gene amplicons for the illumina MiSeq system. San Diego, United States: Illumina Inc, 2013, 28p.

INFANTE, F. et al. Coffee pests. In: ASIEGBU, F. O.; KOVALCHUK, A. Forest microbiology: Tree diseases and pests. London, United Kingdom: Academic Press, p. 213-225, 2022.

INTERNATIONAL COFFEE ORGANIZATION - ICO. Coffee development report (CDR): The future of coffee, Investing in youth for a resilient and sustainable coffee sector. London, United Kingdom: ICO, 2021. 94p.

INVITROGEN. Quant-iTTM PicoGreenTM dsDNA Assay Kit. Waltham, United States: Invitrogen, 2022. 6p. Available in: https://www.thermofisher.com/document-connect/document-connect.html?url=https://assets.thermofisher.com/TFS-Assets%2FLSG%2Fmanuals%2Fmp07581.pdf.> access in: September 6, 2023.

KROONEMAN, J. et al. Lactobacillus diolivorans sp. nov., a 1,2-propanediol-degrading bacterium isolated from aerobically stable maize silage. International Journal of Systematic and Evolutionary Microbiology, 52(2):639-646, 2002.

KUMAR, S.; BROOKS, M. S.-L. Natural deep eutectic solvents for sustainable extraction of pigments and antioxidants from agri-processing waste. In: BHAT, R. Valorization of agri-food wastes and by-products: Recent trends, innovations and sustainability challenges. London, United Kingdom: Academic Press, p.747-785, 2021.

LEONG, K. et al. Diversity of lactic acid bacteria associated with fresh coffee Cherries in Taiwan. Current Microbiology, 68:440-447, 2014.

LIU, D. D.; GU, C. T. Lactobacillus pingfangensis sp. nov., Lactobacillus daoliensis sp. nov., Lactobacillus nangangensis sp. nov., Lactobacillus daowaiensis sp. nov., Lactobacillus dongliensis sp. nov., Lactobacillus songbeiensis sp. nov. and Lactobacillus kaifaensis sp. nov., isolated from traditional Chinese pickle. International Journal of Systematic and Evolutionary Microbiology, 69(10):3237-3247, 2019.

LONG, G. Y. et al. Lactobacillus hegangensis sp. nov., Lactobacillus suibinensis sp. nov., Lactobacillus daqingensis sp. nov., Lactobacillus yichunensis sp. nov., Lactobacillus mulanensis sp. nov., Lactobacillus achengensis sp. nov., Lactobacillus wuchangensis sp. nov., Lactobacillus gannanensis sp. nov., Lactobacillus binensis sp. nov. and Lactobacillus angrenensis sp. nov., isolated from Chinese traditional pickle and yogurt. International Journal of Systematic and Evolutionary Microbiology, 70(4):2467-2484, 2020.

LONG, G. Y.; GU, C. T. Lactobacillus jixianensis sp. nov., Lactobacillus baoqingensis sp. nov., Lactobacillus jiayinensis sp. nov., Lactobacillus zhaoyuanensis sp. nov., Lactobacillus lindianensis sp. nov., Lactobacillus huananensis sp. nov., Lactobacillus tangyuanensis sp. nov., Lactobacillus fuyuanensis sp. nov., Lactobacillus tongjiangensis sp. nov., Lactobacillus fujinensis sp. nov. and Lactobacillus mulengensis sp. nov., isolated from Chinese traditional pickle. International Journal of Systematic and Evolutionary Microbiology, 69(8):2340-2353, 2019.

MARTINS, P. M. M. et al. Coffee growing altitude influences the microbiota, chemical compounds and the quality of fermented coffees. Food Research International, 129:108872, 2020.

MCGORRIN, R. J. The Significance of volatile sulfur compounds in food flavors: An overview. In: QIAN, M. C.; FAN, X.; MAHATTANATAWEE, K. Volatile sulfur compounds in food. Washington, United States: American Chemical Society, v. 1068, p.3-31, 2011.

MUZAIFA, M. et al. Phenotypic identification of lactic acid bacteria from civet (Paradoxorus hermaphroditus). International Journal on Advanced Science, Engineering and Information Technology, 9(5):1681, 2019.

NASANIT, R.; SATAYAWUT, K. Microbiological study during coffee fermentation of Coffea arabica var. chiangmai 80 in Thailand. Kasetsart Journal - Natural Science, 49(1):32-41, 2015.

ONYEAKA, H. N.; NWABOR, O. F. Lactic acid bacteria and bacteriocins as biopreservatives. In: ONYEAKA, H. N.; NWABOR, O. F. Food preservation and safety of natural products. London, United Kingdom: Academic Press, p. 147-162, 2022.

PADONOU, S. W. et al. Weissella beninensis sp. nov., a motile lactic acid bacterium from submerged cassava fermentations, and emended description of the genus Weissella. International Journal of Systematic and Evolutionary Microbiology, 60(9):2193-2198, 2010.

PEÑUELA-MARTÍNEZ, A. E.; MORENO-RIASCOS, S.; MEDINA-RIVERA, R. Influence of temperature-controlled fermentation on the quality of mild coffee (Coffea arabica L.) cultivated at different elevations. Agriculture, 13(6):1132, 2023.

PEÑUELA-MARTÍNEZ, A. E.; VELASQUEZ-EMILIANI, A. V.; ANGEL, C. A. Microbial diversity using a metataxonomic approach, associated with coffee fermentation processes in the department of quindío, Colombia. Fermentation, 9(4):343, 2023.

PEREIRA, L. et al. Relationship between coffee processing and fermentation. In: PEREIRA, L.; MOREIRA, T. Quality determinants in coffee production. Gewerbestrasse, Swirzerland: Springer, p. 255-301, 2021.

PEREIRA, T. S. et al. Self-induced anaerobiosis coffee fermentation: Impact on microbial communities, chemical composition and sensory quality of coffee. Food Microbiology, 103:103962, 2022.

PINO, A. F. S.; ESPINOSA, Z. Y. D.; CABRERA, E. V. R. Characterization of the rhizosphere bacterial microbiome and coffee bean fermentation in the castillo-tambo and bourbon varieties in the popayán-colombia plateau. BMC Plant Biology, 23:217, 2023.

POTHAKOS, V. et al. Temporal shotgun metagenomics of an ecuadorian coffee fermentation process highlights the predominance of lactic acid bacteria. Current Research in Biotechnology, 2:1-15, 2020.

QIAGEN. DNeasy PowerLyzer PowerSoil Kit Handbook. Hilden, Germany: Qiagen, 2020. 27p.

QUAST, C. et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1):D590-D596, 2012.

RIBEIRO, L. S. et al. Microbiological and chemical-sensory characteristics of three coffee varieties processed by wet fermentation. Annals of Microbiology, 68(10):705-716, 2018.

RIBEIRO, L. S. et al. The use of mesophilic and lactic acid bacteria strains as starter cultures for improvement of coffee beans wet fermentation. World Journal of Microbiology and Biotechnology, 36:186, 2020.

SCHLOSS, P. D. et al. Introducing mothur: Open-Source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75(23):7537-7541, 2009.

SCHMIDT, V. S. J. et al. Bavariicoccus seileri gen. nov., sp. nov., isolated from the surface and smear water of German red smear soft cheese. International Journal of Systematic and Evolutionary Microbiology, 59(10):2437-2443, 2009.

SUPERINTENDENCIA DE INDUSTRIA Y COMERCIO - SIC. Denominación de origen Café de la Sierra Nevada: Resolución 2484 de 2017. Bogotá, Colombia: Superintendencia de Industria y Comercio, 2017. 26p. Available in: <https://www.sic.gov.co/sites/default/files/files/Denominacion%20de%20Origen/Resoluci%C3%B3n%202484%20Caf%C3%A9%20de%20la%20Sierra%20Nevada.pdf>. access in: September 6, 2023.

SNAUWAERT, I. et al. Characterization of strains of Weissella fabalis sp. nov. and Fructobacillus tropaeoli from spontaneous cocoa bean fermentations. International Journal of Systematic and Evolutionary Microbiology, 63:1709-1716, 2013.

SUZUKI, K. et al. Lactobacillus paracollinoides sp. nov., isolated from brewery environments. International Journal of Systematic and Evolutionary Microbiology, 54(1):115-117, 2004.

TAMANG, J. P. Biochemical and modern identification techniques: Microfloras of fermented foods. In: BATT, C. A.; TORTORELLO, M. L. Encyclopedia of food microbiology. London, United Kingdom: Academic Press, p. 250-258, 2014.

VILELA, D. M. et al. Molecular ecology and polyphasic characterization of the microbiota associated with semi-dry processed coffee (Coffea arabica L.). Food Microbiology, 27(8):1128-1135, 2010.

WANG, C. et al. Coffee flavour modification through controlled fermentation of green coffee beans by Lactococcus lactis subsp. cremoris. LWT, 120:108930, 2020.

WANG, L.-T. et al. Lactobacillus taiwanensis sp. nov., isolated from silage. International Journal of Systematic and Evolutionary Microbiology, 59(8):2064-2068, 2009.

ZHANG, S. J. et al. Following coffee production from cherries to cup: Microbiological and metabolomic analysis of wet processing of coffea arabica. Applied and Environmental Microbiology, 85(6):e02635-18, 2019.

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Published

2023-10-03

How to Cite

O’BYRNE, R. C.; PIRANEQUE-GAMBASICA, N.; AGUIRRE-FORERO, S. Lactic acid bacteria diversity and dynamics in Colombian coffee fermentation. Coffee Science - ISSN 1984-3909, [S. l.], v. 18, p. e182141, 2023. DOI: 10.25186/.v18i.2141. Disponível em: https://coffeescience.ufla.br/index.php/Coffeescience/article/view/2141. Acesso em: 21 apr. 2024.