Discovering the indigenous microbial communities associated with the natural fermentation of sap from the cider gum Eucalyptus gunnii.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
07 09 2020
07 09 2020
Historique:
received:
10
02
2020
accepted:
19
08
2020
entrez:
8
9
2020
pubmed:
9
9
2020
medline:
29
12
2020
Statut:
epublish
Résumé
Over the course of human history and in most societies, fermented beverages have had a unique economic and cultural importance. Before the arrival of the first Europeans in Australia, Aboriginal people reportedly produced several fermented drinks including mangaitch from flowering cones of Banksia and way-a-linah from Eucalyptus tree sap. In the case of more familiar fermented beverages, numerous microorganisms, including fungi, yeast and bacteria, present on the surface of fruits and grains are responsible for the conversion of the sugars in these materials into ethanol. Here we describe native microbial communities associated with the spontaneous fermentation of sap from the cider gum Eucalyptus gunnii, a Eucalyptus tree native to the remote Central Plateau of Tasmania. Amplicon-based phylotyping showed numerous microbial species in cider gum samples, with fungal species differing greatly to those associated with winemaking. Phylotyping also revealed several fungal sequences which do not match known fungal genomes suggesting novel yeast species. These findings highlight the vast microbial diversity associated with the Australian Eucalyptus gunnii and the native alcoholic beverage way-a-linah.
Identifiants
pubmed: 32895409
doi: 10.1038/s41598-020-71663-x
pii: 10.1038/s41598-020-71663-x
pmc: PMC7477236
doi:
Substances chimiques
DNA, Fungal
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
14716Références
Legras, J. L., Merdinoglu, D., Cornuet, J. M. & Karst, F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol. Ecol. 16, 2091–2102 (2007).
doi: 10.1111/j.1365-294X.2007.03266.x
McGovern, P. E. et al. Fermented beverages of pre- and proto-historic China. Proc. Natl. Acad. Sci. U.S.A. 101, 17593–17598. https://doi.org/10.1073/pnas.0407921102 (2004).
doi: 10.1073/pnas.0407921102
pubmed: 15590771
pmcid: 539767
Cavalieri, D., McGovern, P., Hartl, D., Mortimer, R. & Polsinelli, M. Evidence for S. cerevisiae fermentation in ancient wine. J. Mol. Evol. 57, S226–S232 (2003).
doi: 10.1007/s00239-003-0031-2
McGovern, P., Hartung, U., Badler, V., Glusker, D. & Exner, L. The beginnings of winemaking and viniculture in the ancient Near East and Egypt. Expedition 39, 3–21 (1997).
Dudley, R. Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integr. Comp. Biol. 44, 315–323 (2004).
doi: 10.1093/icb/44.4.315
Dudley, R. Fermenting fruit and the historical ecology of ethanol ingestion: is alcoholism in modern humans an evolutionary hangover?. Addiction 97, 381–388. https://doi.org/10.1046/j.1360-0443.2002.00002.x (2002).
doi: 10.1046/j.1360-0443.2002.00002.x
pubmed: 11964055
Carrigan, M. A. et al. Hominids adapted to metabolize ethanol long before human-directed fermentation. Proc. Natl. Acad. Sci. U.S.A. 112, 458–463. https://doi.org/10.1073/pnas.1404167111 (2015).
doi: 10.1073/pnas.1404167111
pubmed: 25453080
Alba-Lois, L. & Segal-Kischinevzky, C. Yeast fermentation and the making of beer and wine https://www.nature.com/scitable/topicpage/yeast-fermentation-and-the-making-of-beer-14372813 (2010).
Malacarne, M., Martuzzi, F., Summer, A. & Mariani, P. Protein and fat composition of mare’s milk: some nutritional remarks with reference to human and cow’s milk. Int. Dairy J. 12, 869–877. https://doi.org/10.1016/S0958-6946(02)00120-6 (2002).
doi: 10.1016/S0958-6946(02)00120-6
Brady, M. First Taste. How Indigenous Australians Learned About Grog (Alcohol Education and Rehabilitation Foundation Ltd, Canberra, 2008).
Brady, M. & McGrath, V. Making Tuba in the Torres Strait islands: the cultural diffusion and geographic mobility of an alcoholic drink. J. Pac. Hist. 45, 315–330. https://doi.org/10.1080/00223344.2010.530811 (2010).
doi: 10.1080/00223344.2010.530811
pubmed: 21280393
Varela, C. The impact of non-Saccharomyces yeasts in the production of alcoholic beverages. Appl. Microbiol. Biotechnol. 100, 9861–9874. https://doi.org/10.1007/s00253-016-7941-6 (2016).
doi: 10.1007/s00253-016-7941-6
pubmed: 27787587
Jolly, N. P., Varela, C. & Pretorius, I. S. Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res. 14, 215–237. https://doi.org/10.1111/1567-1364.12111 (2014).
doi: 10.1111/1567-1364.12111
pubmed: 24164726
Steinkraus, K. H. Handbook of Indigenous Fermented Foods, Second Edition, Revised and Expanded (Marcel Dekker, New York, 1995).
Tamang, J. P., Watanabe, K. & Holzapfel, W. H. Review: diversity of microorganisms in global fermented foods and beverages. Front. Microbiol. https://doi.org/10.3389/fmicb.2016.00377 (2016).
doi: 10.3389/fmicb.2016.00377
pubmed: 27446012
pmcid: 4914496
Bahiru, B., Mehari, T. & Ashenafi, M. Yeast and lactic acid flora of tej, an indigenous Ethiopian honey wine: variations within and between production units. Food Microbiol. 23, 277–282. https://doi.org/10.1016/j.fm.2005.05.007 (2006).
doi: 10.1016/j.fm.2005.05.007
pubmed: 16943014
Vallejo, J. A. et al. Atypical yeasts identified as Saccharomyces cerevisiae by MALDI-TOF MS and gene sequencing are the main responsible of fermentation of chicha, a traditional beverage from Peru. Syst. Appl. Microbiol. 36, 560–564. https://doi.org/10.1016/j.syapm.2013.09.002 (2013).
doi: 10.1016/j.syapm.2013.09.002
pubmed: 24120265
Puerari, C., Magalhães-Guedes, K. T. & Schwan, R. F. Physicochemical and microbiological characterization of chicha, a rice-based fermented beverage produced by Umutina Brazilian Amerindians. Food Microbiol. 46, 210–217. https://doi.org/10.1016/j.fm.2014.08.009 (2015).
doi: 10.1016/j.fm.2014.08.009
pubmed: 25475287
Escalante, A. et al. Characterization of bacterial diversity in Pulque, a traditional Mexican alcoholic fermented beverage, as determined by 16S rDNA analysis. FEMS Microbiol. Lett. 235, 273–279. https://doi.org/10.1016/j.femsle.2004.04.045 (2004).
doi: 10.1016/j.femsle.2004.04.045
pubmed: 15183874
Lappe-Oliveras, P. et al. Yeasts associated with the production of Mexican alcoholic nondistilled and distilled Agave beverages. FEMS Yeast Res. 8, 1037–1052. https://doi.org/10.1111/j.1567-1364.2008.00430.x (2008).
doi: 10.1111/j.1567-1364.2008.00430.x
pubmed: 18759745
Jung, M. J., Nam, Y. D., Roh, S. W. & Bae, J. W. Unexpected convergence of fungal and bacterial communities during fermentation of traditional Korean alcoholic beverages inoculated with various natural starters. Food Microbiol. 30, 112–123. https://doi.org/10.1016/j.fm.2011.09.008 (2012).
doi: 10.1016/j.fm.2011.09.008
pubmed: 22265291
Greppi, A. et al. Determination of yeast diversity in ogi, mawe, gowe and tchoukoutou by using culture-dependent and -independent methods. Int. J. Food Microbiol. 165, 84–88. https://doi.org/10.1016/j.ijfoodmicro.2013.05.005 (2013).
doi: 10.1016/j.ijfoodmicro.2013.05.005
pubmed: 23727651
Spitaels, F. et al. The microbial diversity of traditional spontaneously fermented lambic beer. PLoS ONE https://doi.org/10.1371/journal.pone.0095384 (2014).
doi: 10.1371/journal.pone.0095384
pubmed: 24748344
pmcid: 3991685
Tapsoba, F., Legras, J. L., Savadogo, A., Dequin, S. & Traore, A. S. Diversity of Saccharomyces cerevisiae strains isolated from Borassus akeassii palm wines from Burkina Faso in comparison to other African beverages. Int. J. Food Microbiol. 211, 128–133. https://doi.org/10.1016/j.ijfoodmicro.2015.07.010 (2015).
doi: 10.1016/j.ijfoodmicro.2015.07.010
pubmed: 26202324
Bokulich, N. A., Bamforth, C. W. & Mills, D. A. Brewhouse-resident microbiota are responsible for multi-stage fermentation of American coolship ale. PLoS ONE 7, e35507. https://doi.org/10.1371/journal.pone.0035507 (2012).
doi: 10.1371/journal.pone.0035507
pubmed: 22530036
pmcid: 3329477
Bokulich, N. A., Thorngate, J. H., Richardson, P. M. & Mills, D. A. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proc. Natl. Acad. Sci. U.S.A. 111, E139–E148. https://doi.org/10.1073/pnas.1317377110 (2014).
doi: 10.1073/pnas.1317377110
pubmed: 24277822
Siren, K. et al. Taxonomic and functional characterization of the microbial community during spontaneous in vitro fermentation of Riesling must. Front. Microbiol. https://doi.org/10.3389/fmicb.2019.00697 (2019).
doi: 10.3389/fmicb.2019.00697
pubmed: 31024486
pmcid: 6465770
Morgan, H. H., du Toit, M. & Setati, M. E. The grapevine and wine microbiome: insights from high-throughput amplicon sequencing. Front. Microbiol. https://doi.org/10.3389/fmicb.2017.00820 (2017).
doi: 10.3389/fmicb.2017.00820
pubmed: 29180986
pmcid: 5693916
Williams, K. J. & Potts, B. M. The natural distribution of Eucalyptus species in Tasmania. Tasforests 8, 39–165 (1996).
Calder, J. A. & Kirkpatrick, J. B. Climate change and other factors influencing the decline of the Tasmanian cider gum (Eucalyptus gunnii). Aust. J. Bot. 56, 684–692. https://doi.org/10.1071/BT08105 (2008).
doi: 10.1071/BT08105
Sanger, J. C., Davidson, N. J., O’Grady, A. P. & Close, D. C. Are the patterns of regeneration in the endangered Eucalyptus gunnii ssp. divaricata shifting in response to climate?. Austral. Ecol. 36, 612–620. https://doi.org/10.1111/j.1442-9993.2010.02194.x (2011).
doi: 10.1111/j.1442-9993.2010.02194.x
Lahti, L. & Shetty, S. Tools for microbiome analysis in R. Version 1.9.1 https://microbiome.github.com/microbiome (2017).
Morrison-Whittle, P. & Goddard, M. R. Quantifying the relative roles of selective and neutral processes in defining eukaryotic microbial communities. ISME J. 9, 2003–2011. https://doi.org/10.1038/ismej.2015.18 (2015).
doi: 10.1038/ismej.2015.18
pubmed: 25756681
pmcid: 4542032
Morrison-Whittle, P. & Goddard, M. R. From vineyard to winery: a source map of microbial diversity driving wine fermentation. Environ. Microbiol. 20, 75–84. https://doi.org/10.1111/1462-2920.13960 (2018).
doi: 10.1111/1462-2920.13960
pubmed: 29052965
Brooker, M. I. H. A Key to Eucalypts in Britain and Ireland. (Forestry Commission Booklet 50: The Stationery Office, 1983).
Forrest, M. & Moore, T. Eucalyptus gunnii: a possible source of bioenergy?. Biomass Bioenerg. 32, 978–980. https://doi.org/10.1016/j.biombioe.2008.01.010 (2008).
doi: 10.1016/j.biombioe.2008.01.010
Guimarães, R. et al. Aromatic plants as a source of important phytochemicals: vitamins, sugars and fatty acids in Cistus ladanifer, Cupressus lusitanica and Eucalyptus gunnii leaves. Ind. Crop Prod. 30, 427–430. https://doi.org/10.1016/j.indcrop.2009.08.002 (2009).
doi: 10.1016/j.indcrop.2009.08.002
Bugarin, D. et al. Essential oil of Eucalyptus gunnii hook. As a novel source of antioxidant, antimutagenic and antibacterial agents. Molecules 19, 19007–19020. https://doi.org/10.3390/molecules191119007 (2014).
doi: 10.3390/molecules191119007
pubmed: 25412046
pmcid: 6271932
Leborgne, N. et al. Introduction of specific carbohydrates into Eucalyptus gunnii cells increases their freezing tolerance. Eur. J. Biochem. 229, 710–717. https://doi.org/10.1111/j.1432-1033.1995.0710j.x (1995).
doi: 10.1111/j.1432-1033.1995.0710j.x
pubmed: 7758467
Stuckel, J. G. & Low, N. H. The chemical composition of 80 pure maple syrup samples produced in North America. Food Res. Int. 29, 373–379. https://doi.org/10.1016/0963-9969(96)00000-2 (1996).
doi: 10.1016/0963-9969(96)00000-2
Taylor, M. W., Tsai, P., Anfang, N., Ross, H. A. & Goddard, M. R. Pyrosequencing reveals regional differences in fruit-associated fungal communities. Environ. Microbiol. 16, 2848–2858 (2014).
doi: 10.1111/1462-2920.12456
Pinto, C. et al. Wine fermentation microbiome: a landscape from different Portuguese wine appellations. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.00905 (2015).
doi: 10.3389/fmicb.2015.00905
pubmed: 26388852
pmcid: 4555975
Miura, T., Sanchez, R., Castaneda, L. E., Godoy, K. & Barbosa, O. Is microbial terroir related to geographic distance between vineyards?. Environ. Microbiol. Rep. 9, 742–749. https://doi.org/10.1111/1758-2229.12589 (2017).
doi: 10.1111/1758-2229.12589
pubmed: 28892290
Knight, S. J., Karon, O. & Goddard, M. R. Small scale fungal community differentiation in a vineyard system. Food Microbiol. https://doi.org/10.1016/j.fm.2019.103358 (2019).
doi: 10.1016/j.fm.2019.103358
pubmed: 31948613
Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688. https://doi.org/10.1126/science.1256688 (2014).
doi: 10.1126/science.1256688
pubmed: 25430773
Lin, Y. T., Whitman, W. B., Coleman, D. C. & Chiu, C. Y. Effects of reforestation on the structure and diversity of bacterial communities in subtropical low mountain forest soils. Front. Microbiol. https://doi.org/10.3389/fmicb.2018.01968 (2018).
doi: 10.3389/fmicb.2018.01968
pubmed: 30692981
pmcid: 6309047
Grangeteau, C. et al. Wine microbiology is driven by vineyard and winery anthropogenic factors. Microb. Biotechnol. 10, 354–370. https://doi.org/10.1111/1751-7915.12428 (2017).
doi: 10.1111/1751-7915.12428
pubmed: 27778455
Burns, K. N. et al. Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: differentiation by geographic features. Soil Biol. Biochem. 91, 232–247. https://doi.org/10.1016/j.soilbio.2015.09.002 (2015).
doi: 10.1016/j.soilbio.2015.09.002
Portillo, M. D. C., Franquès, J., Araque, I., Reguant, C. & Bordons, A. Bacterial diversity of Grenache and Carignan grape surface from different vineyards at Priorat wine region (Catalonia, Spain). Int. J. Food Microbiol. 219, 56–63. https://doi.org/10.1016/j.ijfoodmicro.2015.12.002 (2016).
doi: 10.1016/j.ijfoodmicro.2015.12.002
Castaneda, L. E. & Barbosa, O. Metagenomic analysis exploring taxonomic and functional diversity of soil microbial communities in Chilean vineyards and surrounding native forests. PeerJ 5, e3098. https://doi.org/10.7717/peerj.3098 (2017).
doi: 10.7717/peerj.3098
pubmed: 28382231
pmcid: 5376117
Setati, M. E., Jacobson, D. & Bauer, F. F. Sequence-based analysis of the Vitis vinifera L. cv Cabernet Sauvignon grape must Mycobiome in three South African vineyards employing distinct agronomic systems. Front. Microbiol. https://doi.org/10.3389/fmicb.2015.01358 (2015).
doi: 10.3389/fmicb.2015.01358
pubmed: 26834719
pmcid: 4663253
Miura, T. et al. Shifts in the composition and potential functions of soil microbial communities responding to a no-tillage practice and bagasse mulching on a sugarcane plantation. Biol. Fertil. Soils 52, 307–322. https://doi.org/10.1007/s00374-015-1077-1 (2016).
doi: 10.1007/s00374-015-1077-1
Miura, T., Sanchez, R., Castaneda, L. E., Godoy, K. & Barbosa, O. Shared and unique features of bacterial communities in native forest and vineyard phyllosphere. Ecol. Evol. 9, 3295–3305. https://doi.org/10.1002/ece3.4949 (2019).
doi: 10.1002/ece3.4949
pubmed: 30962893
pmcid: 6434556
Hendgen, M. et al. Effects of different management regimes on microbial biodiversity in vineyard soils. Sci. Rep. https://doi.org/10.1038/s41598-018-27743-0 (2018).
doi: 10.1038/s41598-018-27743-0
pubmed: 29925862
pmcid: 6010416
Montecchia, M. S. et al. Pyrosequencing reveals changes in soil bacterial communities after conversion of Yungas forests to agriculture. PLoS ONE 10, 18. https://doi.org/10.1371/journal.pone.0119426 (2015).
doi: 10.1371/journal.pone.0119426
Gleeson, D., Mathes, F., Farrell, M. & Leopold, M. Environmental drivers of soil microbial community structure and function at the Avon River Critical Zone Observatory. Sci. Total Environ. 571, 1407–1418. https://doi.org/10.1016/j.scitotenv.2016.05.185 (2016).
doi: 10.1016/j.scitotenv.2016.05.185
pubmed: 27432724
Kemler, M. et al. Ion Torrent PGM as tool for fungal community analysis: a case study of Endophytes in Eucalyptus grandis reveals high taxonomic diversity. PLoS ONE https://doi.org/10.1371/journal.pone.0081718 (2013).
doi: 10.1371/journal.pone.0081718
pubmed: 24358124
pmcid: 3864840
Piškur, J., Rozpędowska, E., Polakova, S., Merico, A. & Compagno, C. How did Saccharomyces evolve to become a good brewer?. Trends Genet. 22, 183–186. https://doi.org/10.1016/j.tig.2006.02.002 (2006).
doi: 10.1016/j.tig.2006.02.002
pubmed: 16499989
Lloyd, K. G., Steen, A. D., Ladau, J., Yin, J. Q. & Crosby, L. Phylogenetically novel uncultured microbial cells dominate Earth microbiomes. Msystems https://doi.org/10.1128/mSystems.00055-18 (2018).
doi: 10.1128/mSystems.00055-18
pubmed: 30273414
pmcid: 6156271
Steen, A. D. et al. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J. 13, 3126–3130. https://doi.org/10.1038/s41396-019-0484-y (2019).
doi: 10.1038/s41396-019-0484-y
pubmed: 31388130
pmcid: 6863901
Thrash, J. C. Culturing the uncultured: Risk versus reward. Msystems https://doi.org/10.1128/mSystems.00130-19 (2019).
doi: 10.1128/mSystems.00130-19
pubmed: 31117022
pmcid: 6529549
Varela, C., Pizarro, F. & Agosin, E. Biomass content governs fermentation rate in nitrogen-deficient wine musts. Appl. Environ. Microbiol. 70, 3392–3400. https://doi.org/10.1128/Aem.70.6.3392-3400.2004 (2004).
doi: 10.1128/Aem.70.6.3392-3400.2004
pubmed: 15184136
pmcid: 427798
Parker, M. et al. Factors contributing to interindividual variation in retronasal odor perception from aroma glycosides: The tole of odorant sensory detection threshold, oral microbiota, and hydrolysis in saliva. J. Agric. Food Chem. https://doi.org/10.1021/acs.jafc.9b05450 (2019).
doi: 10.1021/acs.jafc.9b05450
pubmed: 31630520
Bokulich, N. A. & Mills, D. A. Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl. Environ. Microbiol. 79, 2519–2526. https://doi.org/10.1128/AEM.03870-12 (2013).
doi: 10.1128/AEM.03870-12
pubmed: 23377949
pmcid: 3623200
Sternes, P. R., Lee, D., Kutyna, D. R. & Borneman, A. R. A combined meta-barcoding and shotgun metagenomic analysis of spontaneous wine fermentation. bioRxiv https://doi.org/10.1101/098061 (2017).
doi: 10.1101/098061
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).
doi: 10.1093/bioinformatics/btu170
pubmed: 4103590
pmcid: 4103590
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. https://doi.org/10.14806/ej.17.1.200 (2011).
doi: 10.14806/ej.17.1.200
Magoc, T. & Salzberg, S. L. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27, 2957–2963. https://doi.org/10.1093/bioinformatics/btr507 (2011).
doi: 10.1093/bioinformatics/btr507
pubmed: 21903629
pmcid: 3198573
Mahe, F., Rognes, T., Quince, C., de Vargas, C. & Dunthorn, M. Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2, e593. https://doi.org/10.7717/peerj.593 (2014).
doi: 10.7717/peerj.593
pubmed: 25276506
pmcid: 4178461
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336. https://doi.org/10.1038/nmeth.f.303 (2010).
doi: 10.1038/nmeth.f.303
pubmed: 20383131
pmcid: 3156573
McMurdie, P. J. & Holmes, S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217. https://doi.org/10.1371/journal.pone.0061217 (2013).
doi: 10.1371/journal.pone.0061217
pubmed: 23630581
pmcid: 3632530
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.5.4 https://CRAN.R-project.org/package=vegan (2019).
Li, C., Yu, G. & Zhu, C. microbiomeViz—an R package for visualizing microbiome data https://github.com/lch14forever/microbiomeViz (2018).
Kahle, D. & Wickham, H. ggmap: spatial visualization with ggplot2. R J. 5, 144–161 (2013).
doi: 10.32614/RJ-2013-014
Kassambara, A. ggpubr: 'ggplot2' based publication eady plots. R package version 0.2 https://CRAN.R-project.org/package=ggpubr (2018).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (SpringerVerlag, New York, 2009).
doi: 10.1007/978-0-387-98141-3
Team, R. C. R: a language and environment for statistical computing https://www.R-project.org/ (2017).