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      The epiphytic microbiota of sour rot-affected grapes differs minimally from that of healthy grapes, indicating causal organisms are already present on healthy berries

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          Abstract

          Sour rot is a disease complex produced by an interaction between grape berries and various species of yeast and acetic acid bacteria in the presence of Drosophila fruit flies. While yeast and bacteria are consistently found on healthy grape berries worldwide, we explored whether the composition of these epiphytic communities differed depending on the presence or absence of sour rot symptoms. Using high-throughput sequencing, we characterized the microbiome of sour rot-affected grapes from two geographical areas across two years. In 2015 and 2016, both healthy and sour rot-affected berries were collected from commercial and research vineyards in Geneva, NY and commercial vineyards in Tasmania, AUS. In this experiment, all associated organisms grouped together primarily by location, and not by presence/absence of symptoms or cultivar. The predominant difference between asymptomatic and symptomatic samples, regardless of location, was the abundance of Acetobacter species, which were significantly more plentiful in the symptomatic samples. Yeast genera such as Candida, Hanseniaspora, Pichia and Saccharomyces were abundant in both sets of samples, but varied by region. The consistent presence of yeast species and the increased abundance of acetic acid-generating bacteria is consistent with our understanding of their etiological role in sour rot development. In 2016, diseased grapes also were collected from vineyards in Fredonia, NY, and Modesto, CA. Consistent with our comparison study, all associated organisms again grouped together primarily by location. Yeast genera such as Candida, Hanseniaspora, Pichia and Saccharomyces were abundant in both sets of samples, but varied by region. The consistent presence of yeast species and the abundance of acetic acid-generating bacteria in both experiments is consistent with our understanding of their etiological role in sour rot development.

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

              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.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – original draft
                Role: Formal analysisRole: Software
                Role: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Supervision
                Role: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 March 2019
                2019
                : 14
                : 3
                : e0211378
                Affiliations
                [1 ] Section of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, NYS Agricultural Experiment Station, Geneva, New York, United States of America
                [2 ] Thomas H. Gosnell School of Life Sciences, Rochester Institute of Technology, Rochester, New York, United States of America
                [3 ] United States Department of Agriculture–Agricultural Research Service, Grape Genetics Research Unit, Geneva, New York, United States of America
                University of California Davis, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: Division of Plant Sciences, University of Missouri, Columbia, Missouri, United States of America

                Author information
                http://orcid.org/0000-0001-8301-6128
                Article
                PONE-D-18-30623
                10.1371/journal.pone.0211378
                6436683
                30917111
                2683b3ca-5254-4236-a95b-97ee1aab53b7

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 22 October 2018
                : 12 January 2019
                Page count
                Figures: 5, Tables: 3, Pages: 12
                Funding
                This work was supported the NY State Dept. of Agriculture and Markets (WF), NY Wine and Grape Foundation (WF), Specialty Crops Research Initiative (WF) and the Dyson Fund (WF). Mention of trade names or commercial products is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). USDA is an equal opportunity provider and employer.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Grapes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Fungi
                Yeast
                Biology and Life Sciences
                Organisms
                Bacteria
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Berries
                Earth Sciences
                Marine and Aquatic Sciences
                Bodies of Water
                Lakes
                Ecology and Environmental Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Earth Sciences
                Marine and Aquatic Sciences
                Aquatic Environments
                Freshwater Environments
                Lakes
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Saccharomyces Cerevisiae
                Research and Analysis Methods
                Model Organisms
                Saccharomyces Cerevisiae
                Biology and Life Sciences
                Organisms
                Eukaryota
                Fungi
                Yeast
                Saccharomyces
                Saccharomyces Cerevisiae
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Yeast and Fungal Models
                Saccharomyces Cerevisiae
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Physical Sciences
                Chemistry
                Chemical Compounds
                Acids
                Acetic Acid
                Custom metadata
                Data are available via the Sequence Read Archive, accession number: PRJNA523253.

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