Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages

  Bokulich, Nicholas A ^a   Thorngate, John H ^b   Richardson, Paul M ^c   Mills, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Constellation Brands Inc ^*  (United States)

^c MicroTrek Inc   (United States)

Author keywords

Agriculture; Metagenomics; Next generation sequencing; Viticulture

Indexed keywords

ARTICLE; AUREOBASIDIUM PULLULANS; BACILLALES; BIOGEOGRAPHY; BOTRYTIS CINEREA; CANDIDA; CANDIDA ZEMPLININA; CLADOSPORIUM HERBARUM; CLIMATE; CONTROLLED STUDY; CULTIVAR; ECOLOGY; ENTEROBACTERIALES; ERYSIPHE NECATOR; EVAPOTRANSPIRATION; FERMENTATION; GEOGRAPHIC DISTRIBUTION; GLUCONOBACTER; GRAPE; GRAPE MUST; HANSENIASPORA; HANSENIASPORA UVARUM; HIGH TEMPERATURE; HUMIDITY; LACTOBACILLALES; LATITUDE; LONGITUDE; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MICROBIAL CONSORTIUM; NONHUMAN; PENICILLIUM; PRIORITY JOURNAL; PSEUDOMONADALES; SACCHAROMYCES CEREVISIAE; SOIL TEMPERATURE; WINE;

AGRICULTURE; METAGENOMICS; NEXT-GENERATION SEQUENCING; VITICULTURE;

AGRICULTURE; BIODIVERSITY; CLIMATE; ENVIRONMENT; FERMENTATION; FOOD MICROBIOLOGY; GENOMICS; GEOGRAPHY; PHYLOGENY; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; VITIS; WINE;

EID: 84891933123     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1317377110     Document Type: Article

References (68)

1. Martiny JB, et al. (2006) Microbial biogeography: Putting microorganisms on the map. Nat Rev Microbiol 4(2): 102-112.
2. Koren O, et al. (2012) Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150(3): 470-480.
3. Gibbons SM, et al. (2013) Evidence for a persistent microbial seed bank throughout the global ocean. Proc Natl Acad Sci USA 110(12): 4651-4655.
4. Adams RI, Miletto M, Taylor JW, Bruns TD (2013) Dispersal in microbes: Fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. ISME J 7(7): 1262-1273.
5. Peiffer JA, et al. (2013) Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci USA 110(16): 6548-6553.
6. Barata A, Malfeito-Ferreira M, Loureiro V (2012) The microbial ecology of wine grape berries. Int J Food Microbiol 153(3): 243-259.
7. Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie van Leeuwenhoek 76(1-4): 317-331.
8. Swiegers JH, Bartowsky E, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11(2): 139-173.
9. Van Leeuwen C, Seguin G (2006) The concept of terroir in viticulture. J Wine Res 17(1): 1-10.
10. Renouf V, Claisse O, Lonvaud-Funel A (2007) Inventory and monitoring of wine microbial consortia. Appl Microbiol Biotechnol 75(1): 149-164.
11. Jackson DI, Lombard PB (1993) Environmental and management practices affecting grape composition and wine quality-a review. Am J Enol Vitic 44(4): 409-430.
12. Hong Y-S, et al. (2011) Metabolic influence of Botrytis cinerea infection in champagne base wine. J Agric Food Chem 59(13): 7237-7245.
13. Tosi E, et al. (2013) Induction of grape botrytization during withing affects volatile composition of Recioto di Soave, a "passito"-style wine. Eur Food Res Technol 236: 853-862.
14. Bokulich NA, Joseph CML, Allen GR, Benson A, Mills DA (2012) Next-generation sequencing reveals significant bacterial diversity of botrytized wine. PLoS ONE 7(5): e36357.
15. Barata A, González S, Malfeito-Ferreira M, Querol A, Loureiro V (2008) Sour rotdamaged grapes are sources of wine spoilage yeasts. FEMS Yeast Res 8(7): 1008-1017.
16. Joyeux A, Lafon-Lafourcade S, Ribéreau-Gayon P (1984) Evolution of acetic acid bacteria during fermentation and storage of wine. Appl Environ Microbiol 48(1): 153-156.
17. Ciani M, Comitini F, Mannazzu I, Domizio P (2010) Controlled mixed culture fermentation: A new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10(2): 123-133.
18. Gayevskiy V, Goddard MR (2012) Geographic delineations of yeast communities and populations associated with vines and wines in New Zealand. ISME J 6(7): 1281-1290.
19. Bokulich NA, Mills DA Next-generation approaches to the microbial ecology of food fermentationsBMB Rep(2012) 457377-389.
20. Bokulich NA, Bamforth CW, Mills DA (2012) A review of molecular methods for microbial community profiling of beer and wine. J. Am. Soc. Brew. Chem. 70: 150-162.
21. Humblot C, Guyot J-P (2009) Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl Environ Microbiol 75(13): 4354-4361.
22. Roh SW, et al. (2010) Investigation of archaeal and bacterial diversity in fermented seafood using barcoded pyrosequencing. ISME J 4(1): 1-16.
23. Alegría A, Szczesny P, Mayo B, Bardowski J, Kowalczyk M (2012) Biodiversity in Oscypek, a traditional Polish cheese, determined by culture-dependent and -independent approaches. Appl Environ Microbiol 78(6): 1890-1898.
24. Bokulich NA, Bamforth CW, Mills DA (2012) Brewhouse-resident microbiota are responsible for multi-stage fermentation of American coolship ale. PLoS ONE 7(4): e35507.
25. Bokulich NA, Mills DA (2013) Facility-specific "house" microbiome drives microbial landscapes of artisan cheesemaking plants. Appl Environ Microbiol 79(17): 5214-5223.
26. Bokulich NA, Ohta M, Richardson PM, Mills DA (2013) Monitoring seasonal changes in winery-resident microbiota. PLoS ONE 8(6):e66437.
27. De Filippis F, La Storia A, Villani F, Ercolini D (2013) Exploring the sources of bacterial spoilers in beefsteaks by culture-independent high-throughput sequencing. PLoS ONE 8(7):e70222.
28. Lozupone CA, Knight R (2005) UniFrac: A new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12): 8228-8235.
29. Pereira GE, et al. (2005) 1H NMR and chemometrics to characterize mature grape berries in four wine-growing areas in Bordeaux, France. J Agric Food Chem 53(16): 6382-6389.
30. Son HS, et al. (2009) Metabolomic studies on geographical grapes and their wines using 1H NMR analysis coupled with multivariate statistics. J Agric Food Chem 57(4): 1481-1490.
31. López-Rituerto E, et al. (2012) Investigations of La Rioja terroir for wine production using 1H NMR metabolomics. J Agric Food Chem 60(13): 3452-3461.
32. Fischer U, Roth D, Christmann M (1999) The impact of geographic origin, vintage, and wine estate on sensory properties of Vitis vinifera cv. Riesling wines. Food Qual Prefer 10: 281-288.
33. Robinson AL, et al. (2012) Influence of geographic origin on the sensory characteristics and wine composition of Vitis vinifera cv. Cabernet sauvignon wines from Australia. Am J Enol Vitic 63(4): 467-476.
34. Fleet GH (2008) Wine yeasts for the future. FEMS Yeast Res 8(7): 979-995.
35. Sabate J, Cano J, Esteve-Zarzoso B, Guillamón JM (2002) Isolation and identification of yeasts associated with vineyard and winery by RFLP analysis of ribosomal genes and mitochondrial DNA. Microbiol Res 157(4): 267-274.
36. Cordero-Bueso G, et al. (2011) Influence of the farming system and vine variety on yeast communities associated with grape berries. Int J Food Microbiol 145(1): 132-139.
37. Renouf V, Claisse O, Lonvaud-Funel A (2005) Understanding the microbial ecosystemon the grape berry surface through numeration and identification of yeast and bacteria. Aust J Grape Wine Res 11: 316-327.
38. Fung RW, et al. (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol 146(1): 236-249.
39. Smith RJ (2003) Zinfandel. Wine Grape Varieties in California, ed Christensen LP (University of California Agriculture and Natural Resources, Oakland, CA).
40. Barata A, Malfeito-Ferreira M, Loureiro V (2012) Changes in sour rotten grape berry microbiota during ripening and wine fermentation. Int J FoodMicrobiol 154(3): 152-161.
41. Pereira GE, et al. (2006) Microclimate influence on mineral and metabolic profiles of grape berries. J Agric Food Chem 54(18): 6765-6775.
42. Holt HE, Francis IL, Field J, Herderich MJ, Iland PG (2008) Relationships between berry size, berry phenolic composition and wine quality scores for Cabernet Sauvignon (Vitis viniferaL.) from different pruning treatments and different vintages. Aust J Grape Wine Res 14(3): 191-202.
43. Tofalo R, et al. (2012) Diversity of Candida zemplinina strains from grapes and Italian wines. Food Microbiol 29(1): 18-26.
44. Austin CN, Grove GG, Meyers JM, Wilcox WF (2011) Powdery mildew severity as a function of canopy density: Associated impacts on sunlight penetration and spray coverage. Am J Enol Vitic 62(1): 23-31.
45. Hannah L, et al. (2013) Climate change, wine, and conservation. Proc Natl Acad Sci USA 110(17): 6907-6912.
46. Burie JB, Langlais M, Calonnec A (2011) Switching from a mechanistic model to a continuous model to study at different scales the effect of vine growth on the dynamic of a powdery mildew epidemic. Ann Bot (Lond) 107(5): 885-895.
47. Pugliese M, Gullino ML, Garibaldi A Effect of climate change on infection of grapevine by downy and powdery mildew under controlled environmentCommun Agric Appl Biol Sci(2011) 764579-582.
48. Weber E, Gubler D, Derr A Powdery mildew controlled with fewer fungicide applications. Practical Winery & Vineyard (January/February).
49. Pfender WF, Gent DH, Mahaffee WF, Coop LB, Fox AD (2011) Decision aids for multiple- decision disease management as affected by weather input errors. Phytopathology 101(6): 644-653.
50. Fernández-González M, et al. (2012) Forecasting ARIMA models for atmospheric vineyard pathogens in Galicia and Northern Portugal: Botrytis cinerea spores. Ann Agric Environ Med 19(2): 255-262.
51. Larsen PE, Field D, Gilbert JA (2012) Predicting bacterial community assemblages using an artificial neural network approach. Nat Methods 9(6): 621-625.
52. Setati ME, Jacobson D, Andong UC, Bauer F (2012) The vineyard yeast microbiome, a mixed model microbial map. PLoS ONE 7(12):e52609.
53. Bokulich NA, Mills DA (2013) Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol 79(8): 2519-2526.
54. Caporaso JG, et al. (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci USA 108(Suppl 1): 4516-4522.
55. Caporaso JG, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5): 335-336.
56. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19): 2460-2461.
57. DeSantis TZ, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72(7): 5069-5072.
58. Abarenkov K, et al. (2010) The UNITE database for molecular identification of fungi- recent updates and future perspectives. New Phytol 186(2): 281-285.
59. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16): 5261-5267.
60. Caporaso JG, et al. (2010) PyNAST: A flexible tool for aligning sequences to a template alignment. Bioinformatics 26(2): 266-267.
61. Haas BJ, et al.; Human Microbiome Consortium (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21(3): 494-504.
62. Price MN, Dehal PS, Arkin AP (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490.
63. Bokulich NA, et al. (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10(1): 57-59.
64. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18: 117-143.
65. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
66. Liaw A, WeinerM(2002) Classification and regression by RandomForest.RNews 2(3): 18-22.
67. Segata N, et al. (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12(6):R60.
68. Parks DH, et al. (2013) GenGIS 2: Geospatial analysis of traditional and genetic biodiversity, with new gradient algorithms and an extensible plugin framework. PLoS ONE 8(7):e69885.