Grape Sour Rot: A Four-Way Interaction Involving the Host, Yeast, Acetic Acid Bacteria, and Insects

Sour rot, a disease affecting berries of cultivated Vitis spp. worldwide, has not been clearly defined. Reported symptoms of the disease include browning of the berry skin, oozing of disintegrated berry pulp, and the smell of acetic acid, all in the presence of fruit flies (Drosophila spp.). We determined acetic acid concentrations in multiple collections of symptomatic berries, isolated and identified microbes from them, and inoculated commonly isolated organisms into healthy berries with and without concurrent exposure to wild-type or axenic Drosophila melanogaster. Coinoculations combining one of several yeasts (Metschnikowia spp., Pichia spp., and a Saccharomyces sp.) plus an acetic acid bacterium (an Acetobacter sp. and Gluconobacter spp.) reproduced sour rot symptoms, defined here as decaying berries with a loss of turgor and containing acetic acid at a minimum of 0.83 g/liter, based on observed field levels. Symptoms developed only in the presence of D. melanogaster, either wild type or axenic, indicating a nonmicrobial contribution of these insects in addition to a previously suggested microbial role. We conclude that sour rot is the culmination of coinfection by various yeasts, which convert grape sugars to ethanol, and bacteria that oxidize the ethanol to acetic acid, and that this process is mediated by Drosophila spp.