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      Associations among Wine Grape Microbiome, Metabolome, and Fermentation Behavior Suggest Microbial Contribution to Regional Wine Characteristics

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          ABSTRACT

          Regionally distinct wine characteristics ( terroir) are an important aspect of wine production and consumer appreciation. Microbial activity is an integral part of wine production, and grape and wine microbiota present regionally defined patterns associated with vineyard and climatic conditions, but the degree to which these microbial patterns associate with the chemical composition of wine is unclear. Through a longitudinal survey of over 200 commercial wine fermentations, we demonstrate that both grape microbiota and wine metabolite profiles distinguish viticultural area designations and individual vineyards within Napa and Sonoma Counties, California. Associations among wine microbiota and fermentation characteristics suggest new links between microbiota, fermentation performance, and wine properties. The bacterial and fungal consortia of wine fermentations, composed from vineyard and winery sources, correlate with the chemical composition of the finished wines and predict metabolite abundances in finished wines using machine learning models. The use of postharvest microbiota as an early predictor of wine chemical composition is unprecedented and potentially poses a new paradigm for quality control of agricultural products. These findings add further evidence that microbial activity is associated with wine terroir.

          IMPORTANCE

          Wine production is a multi-billion-dollar global industry for which microbial control and wine chemical composition are crucial aspects of quality. Terroir is an important feature of consumer appreciation and wine culture, but the many factors that contribute to terroir are nebulous. We show that grape and wine microbiota exhibit regional patterns that correlate with wine chemical composition, suggesting that the grape microbiome may influence terroir. In addition to enriching our understanding of how growing region and wine properties interact, this may provide further economic incentive for agricultural and enological practices that maintain regional microbial biodiversity.

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          Most cited references30

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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            The Soil Microbiome Influences Grapevine-Associated Microbiota

            ABSTRACT Grapevine is a well-studied, economically relevant crop, whose associated bacteria could influence its organoleptic properties. In this study, the spatial and temporal dynamics of the bacterial communities associated with grapevine organs (leaves, flowers, grapes, and roots) and soils were characterized over two growing seasons to determine the influence of vine cultivar, edaphic parameters, vine developmental stage (dormancy, flowering, preharvest), and vineyard. Belowground bacterial communities differed significantly from those aboveground, and yet the communities associated with leaves, flowers, and grapes shared a greater proportion of taxa with soil communities than with each other, suggesting that soil may serve as a bacterial reservoir. A subset of soil microorganisms, including root colonizers significantly enriched in plant growth-promoting bacteria and related functional genes, were selected by the grapevine. In addition to plant selective pressure, the structure of soil and root microbiota was significantly influenced by soil pH and C:N ratio, and changes in leaf- and grape-associated microbiota were correlated with soil carbon and showed interannual variation even at small spatial scales. Diazotrophic bacteria, e.g., Rhizobiaceae and Bradyrhizobium spp., were significantly more abundant in soil samples and root samples of specific vineyards. Vine-associated microbial assemblages were influenced by myriad factors that shape their composition and structure, but the majority of organ-associated taxa originated in the soil, and their distribution reflected the influence of highly localized biogeographic factors and vineyard management.
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              Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate.

              Wine grapes present a unique biogeography model, wherein microbial biodiversity patterns across viticultural zones not only answer questions of dispersal and community maintenance, they are also an inherent component of the quality, consumer acceptance, and economic appreciation of a culturally important food product. On their journey from the vineyard to the wine bottle, grapes are transformed to wine through microbial activity, with indisputable consequences for wine quality parameters. Wine grapes harbor a wide range of microbes originating from the surrounding environment, many of which are recognized for their role in grapevine health and wine quality. However, determinants of regional wine characteristics have not been identified, but are frequently assumed to stem from viticultural or geological factors alone. This study used a high-throughput, short-amplicon sequencing approach to demonstrate that regional, site-specific, and grape-variety factors shape the fungal and bacterial consortia inhabiting wine-grape surfaces. Furthermore, these microbial assemblages are correlated to specific climatic features, suggesting a link between vineyard environmental conditions and microbial inhabitation patterns. Taken together, these factors shape the unique microbial inputs to regional wine fermentations, posing the existence of nonrandom "microbial terroir" as a determining factor in regional variation among wine grapes.
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                Author and article information

                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                14 June 2016
                May-Jun 2016
                : 7
                : 3
                : e00631-16
                Affiliations
                [a ]Department of Food Science and Technology, University of California, Davis, California, USA
                [b ]Department of Viticulture and Enology, University of California, Davis, California, USA
                [c ]Foods for Health Institute, University of California, Davis, California, USA
                [d ]Food Safety and Measurement Facility, University of California, Davis, California, USA
                [e ]Far Niente and Nickel & Nickel Wineries, Oakville, California, USA
                Author notes
                Address correspondence to David A. Mills, damills@ 123456ucdavis.edu .
                [*]

                Present address: Nicholas A. Bokulich, Center for Microbial Genetics and Genomics, Northern Arizona University, Flagstaff, Arizona, USA; Thomas S. Collins, Viticulture and Enology Program, Washington State University, Richland, Washington, USA.

                Editor Steven E. Lindow, University of California, Berkeley

                Article
                mBio00631-16
                10.1128/mBio.00631-16
                4959672
                27302757
                cd222de9-8302-4bc2-a38c-5b71785f237f
                Copyright © 2016 Bokulich et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 5 May 2016
                : 9 May 2016
                Page count
                supplementary-material: 9, Figures: 7, Tables: 1, Equations: 0, References: 48, Pages: 12, Words: 9225
                Funding
                This work, including the efforts of Nicholas Andrew Bokulich, was funded in part by HHS | NIH | National Institute of General Medical Sciences (NIGMS) (T32-GM008799) and the Louise and Ray Rossi Endowment to the Department of Viticulture and Enology at UC Davis.
                Categories
                Research Article
                Custom metadata
                May/June 2016

                Life sciences
                Life sciences

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