Wine terroir and the soil microbiome: an amplicon sequencing–based assessment of the Barossa Valley and its sub-regions

Soil is an important factor that contributes to the uniqueness of a wine produced by vines grown in specific conditions. Recent data shows that the composition, diversity and function of soil microbial communities may play important roles in determining wine quality and indirectly affect its economic value. Here, we evaluated the impact of environmental variables on the soil microbiomes of 22 Barossa Valley vineyard sites based on the 16S rRNA gene hypervariable region 4. In this study, we report that environmental heterogeneity (soil plant-available P content, elevation, rainfall, temperature, spacing between row and spacing between vine) caused more microbial dissimilarity than geographic distance. Vineyards located in cooler and wetter regions showed lower beta diversity and a higher ratio of dominant taxa. Differences in microbial community composition were significantly associated with differences in fruit traits and in wine chemical and metabolomic profiles, highlighting the potential influence of microbial communities on the phenotype of grapevines. Our results suggest that environmental factors affect wine terroir, and this may be mediated by changes in microbial structure, thus providing a basic understanding of how growing conditions affect interactions between plants and their soil microbiomes.

[1]  G. Rajivgandhi,et al.  Soil Microbiome , 2021, Microbiome-Host Interactions.

[2]  William A. Walters,et al.  Large-scale replicated field study of maize rhizosphere identifies heritable microbes , 2018, Proceedings of the National Academy of Sciences.

[3]  Andrea Galimberti,et al.  Geographical and Cultivar Features Differentiate Grape Microbiota in Northern Italy and Spain Vineyards , 2018, Front. Microbiol..

[4]  D. Huggins,et al.  Altered Bacterial Communities in Long-Term No-Till Soils Associated with Stratification of Soluble Aluminum and Soil pH , 2018 .

[5]  M. V. D. van der Heijden,et al.  Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming , 2018, Microbiome.

[6]  O. Barbosa,et al.  Is microbial terroir related to geographic distance between vineyards? , 2017, Environmental microbiology reports.

[7]  Timothy R. Cavagnaro,et al.  A Concise Review on Multi-Omics Data Integration for Terroir Analysis in Vitis vinifera , 2017, Front. Plant Sci..

[8]  T. Cavagnaro,et al.  Environmental conditions and agronomic practices induce consistent global changes in DNA methylation patterns in grapevine (Vitis vinifera cv Shiraz) , 2017, bioRxiv.

[9]  Zhenfa Zhang,et al.  pH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution , 2017, Scientific Reports.

[10]  Fiona Curran-Cournane,et al.  Bacteria as Emerging Indicators of Soil Condition , 2016, Applied and Environmental Microbiology.

[11]  Youzhi Feng,et al.  Consistent responses of the microbial community structure to organic farming along the middle and lower reaches of the Yangtze River , 2016, Scientific Reports.

[12]  P. Botía,et al.  Interannual climatic variability effects on yield, berry and wine quality indices in long-term deficit irrigated grapevines, determined by multivariate analysis , 2016 .

[13]  S. Tringe,et al.  Host genotype and age shape the leaf and root microbiomes of a wild perennial plant , 2016, Nature Communications.

[14]  David A. Mills,et al.  Associations among Wine Grape Microbiome, Metabolome, and Fermentation Behavior Suggest Microbial Contribution to Regional Wine Characteristics , 2016, mBio.

[15]  D. Edwards,et al.  The impact of tropical forest logging and oil palm agriculture on the soil microbiome , 2016, Molecular ecology.

[16]  T. Cavagnaro Life at the interface: above- and below-ground responses of a grazed pasture soil to reforestation , 2016 .

[17]  N. Bokulich,et al.  Vineyard soil bacterial diversity and composition revealed by 16S rRNA genes: Differentiation by geographic features , 2015 .

[18]  Jizhong Zhou,et al.  Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession , 2015, Scientific Reports.

[19]  W. Liesack,et al.  Differential Assemblage of Functional Units in Paddy Soil Microbiomes , 2015, PloS one.

[20]  Howard Wildman,et al.  Improving Mine Rehabilitation Success Through Microbial Management , 2015 .

[21]  David A. Mills,et al.  The Soil Microbiome Influences Grapevine-Associated Microbiota , 2015, mBio.

[22]  F. D. Andreote,et al.  Bacterial communities in the rhizosphere of Vitis vinifera L. cultivated under distinct agricultural practices in Argentina , 2014, Antonie van Leeuwenhoek.

[23]  Minou Yussefi-Menzler The World of Organic Agriculture , 2014 .

[24]  L. Seldin,et al.  Plant age and genotype affect the bacterial community composition in the tuber rhizosphere of field-grown sweet potato plants. , 2014, FEMS microbiology ecology.

[25]  M. Schloter,et al.  Dynamics of Soil Bacterial Communities in Response to Repeated Application of Manure Containing Sulfadiazine , 2014, PloS one.

[26]  H. Chu,et al.  High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China , 2014 .

[27]  Rob Knight,et al.  EMPeror: a tool for visualizing high-throughput microbial community data , 2013, GigaScience.

[28]  P. Lemanceau,et al.  Going back to the roots: the microbial ecology of the rhizosphere , 2013, Nature Reviews Microbiology.

[29]  A. Lonvaud,et al.  Characterization of Epiphytic Bacterial Communities from Grapes, Leaves, Bark and Soil of Grapevine Plants Grown, and Their Relations , 2013, PloS one.

[30]  Donovan H. Parks,et al.  GenGIS 2: Geospatial Analysis of Traditional and Genetic Biodiversity, with New Gradient Algorithms and an Extensible Plugin Framework , 2013, PloS one.

[31]  J. V. van Elsas,et al.  Different Selective Effects on Rhizosphere Bacteria Exerted by Genetically Modified versus Conventional Potato Lines , 2013, PloS one.

[32]  Matthew G. Bakker,et al.  Potential impact of soil microbiomes on the leaf metabolome and on herbivore feeding behavior. , 2013, The New phytologist.

[33]  J. Thioulouse,et al.  Turnover of soil bacterial diversity driven by wide-scale environmental heterogeneity , 2013, Nature Communications.

[34]  Scott C Edmunds,et al.  Peering into peer-review at GigaScience , 2013, GigaScience.

[35]  Dweipayan Goswami,et al.  Plant growth promoting potentials of Pseudomonas spp. strain OG isolated from marine water , 2013 .

[36]  N. Spencer,et al.  Advancing our understanding , 2012 .

[37]  Rod Peakall,et al.  GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update , 2012, Bioinform..

[38]  M. Malfeito-Ferreira,et al.  The microbial ecology of wine grape berries. , 2012, International journal of food microbiology.

[39]  Eric P. Nawrocki,et al.  An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea , 2011, The ISME Journal.

[40]  M. Alguacil,et al.  Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. , 2011, Ecological applications : a publication of the Ecological Society of America.

[41]  B. Mitter,et al.  Endophytes of Grapevine Flowers, Berries, and Seeds: Identification of Cultivable Bacteria, Comparison with Other Plant Parts, and Visualization of Niches of Colonization , 2011, Microbial Ecology.

[42]  Rob Knight,et al.  Examining the global distribution of dominant archaeal populations in soil , 2011, The ISME Journal.

[43]  J. Vivanco,et al.  Pyrosequencing Assessment of Soil Microbial Communities in Organic and Conventional Potato Farms. , 2010, Plant disease.

[44]  Jizhong Zhou,et al.  Effects of soil type and farm management on soil ecological functional genes and microbial activities , 2010, The ISME Journal.

[45]  Ramón Mira de Orduña,et al.  Climate change associated effects on grape and wine quality and production , 2010 .

[46]  M. Strand,et al.  Organic agriculture promotes evenness and natural pest control , 2010, Nature.

[47]  William A. Walters,et al.  Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample , 2010, Proceedings of the National Academy of Sciences.

[48]  A. C. Alves,et al.  Influence of Soil Characteristics on the Diversity of Bacteria in the Southern Brazilian Atlantic Forest , 2010, Applied and Environmental Microbiology.

[49]  R. Knight,et al.  Soil bacterial and fungal communities across a pH gradient in an arable soil , 2010, The ISME Journal.

[50]  C. Schadt,et al.  Soil Microbial Community Responses to Multiple Experimental Climate Change Drivers , 2009, Applied and Environmental Microbiology.

[51]  Rob Knight,et al.  PyNAST: a flexible tool for aligning sequences to a template alignment , 2009, Bioinform..

[52]  J. Tiedje,et al.  Changes in land use alter the structure of bacterial communities in Western Amazon soils , 2009, The ISME Journal.

[53]  R. Knight,et al.  Pyrosequencing-Based Assessment of Soil pH as a Predictor of Soil Bacterial Community Structure at the Continental Scale , 2009, Applied and Environmental Microbiology.

[54]  W. Verstraete,et al.  Initial community evenness favours functionality under selective stress , 2009, Nature.

[55]  J. Wiegel,et al.  Diversity of Thermophilic Anaerobes , 2008, Annals of the New York Academy of Sciences.

[56]  J. Vivanco,et al.  Root Exudates Regulate Soil Fungal Community Composition and Diversity , 2007, Applied and Environmental Microbiology.

[57]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[58]  Eoin L. Brodie,et al.  Greengenes: Chimera-checked 16S rRNA gene database and workbench compatible in ARB , 2006 .

[59]  R. B. Jackson,et al.  The diversity and biogeography of soil bacterial communities. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Knight,et al.  UniFrac: a New Phylogenetic Method for Comparing Microbial Communities , 2005, Applied and Environmental Microbiology.

[61]  Tore Krogstad,et al.  Influence of chemically and biologically stabilized sewage sludge on plant-available phosphorous in soil , 2005 .

[62]  S. Frey,et al.  Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests , 2004 .

[63]  P. Nannipieri,et al.  Microbial diversity and soil functions , 2003 .

[64]  P. Nannipieri,et al.  Microbial diversity and soil functions , 2003 .

[65]  P. Dry,et al.  Response of Shiraz grapevines to five different training systems in the Barossa Valley, Australia , 2003 .

[66]  D. Lotter,et al.  Organic Agriculture , 2003 .

[67]  J. Pretty,et al.  Soil Type Is the Primary Determinant of the Composition of the Total and Active Bacterial Communities in Arable Soils , 2003, Applied and Environmental Microbiology.

[68]  D. Wardle,et al.  Spatial soil ecology , 2002 .

[69]  E. Kandeler,et al.  Microbial Population Structures in Soil Particle Size Fractions of a Long-Term Fertilizer Field Experiment , 2001, Applied and Environmental Microbiology.

[70]  P. Kardol,et al.  Bacterial community dynamics in the rhizosphere of a long-lived, leguminous shrub across a 40-year age sequence , 2017, Journal of Soils and Sediments.

[71]  A. Schmalenberger,et al.  Bacterial Mobilization of Nutrients From Biochar-Amended Soils. , 2016, Advances in applied microbiology.

[72]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[73]  R. Bramley,et al.  Choosing biological indicators for monitoring vineyard soil quality , 2014 .

[74]  Rob Knight,et al.  Advancing our understanding of the human microbiome using QIIME. , 2013, Methods in enzymology.

[75]  H. Nayyar,et al.  Synergy between Plants and P-Solubilizing Microbes in soils: Effects on Growth and Physiology of Crops , 2011 .

[76]  S. Siciliano,et al.  Effects of plant species richness and evenness on soil microbial community diversity and function , 2010, Plant and Soil.

[77]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010 .

[78]  Access the most recent version at doi: 10.1101/gr.095612.109 Supplemental Material P , 2009 .

[79]  N. Fierer Microbial Biogeography: Patterns in Microbial Diversity across Space and Time , 2008 .

[80]  Cornelis van Leeuwen,et al.  Influence of Climate, Soil, and Cultivar on Terroir , 2004, American Journal of Enology and Viticulture.

[81]  G. E. Rayment,et al.  Australian laboratory handbook of soil and water chemical methods. , 1992 .

[82]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .