Patulin Inhibition of Specific Apple Microbiome Members Uncovers <i>Hanseniaspora uvarum</i> as a Potential Biocontrol Agent

<i>Penicillium expansum</i> is a major postharvest pathogen of apples, causing loss in fruits through tissue damage, as well as in apple products due to contamination with the mycotoxin patulin. During infections, patulin is a cultivar-dependent virulence factor that facilitates apple lesion development. Patulin also has characterized antimicrobial activity and is important for inhibiting other competitive phytopathogens, but the role of this inhibitory activity has not been investigated in the context of the apple microbiome. In our current study, we isolated 68 apple microbiota and characterized their susceptibility to <i>P</i>. <i>expansum</i> extracts. We found gram-negative bacteria and basidiomycete yeast to demonstrate largely patulin-specific growth inhibition compared with gram-positive and ascomycete isolates. From co-cultures, we identified a <i>Hanseniaspora</i> and <i>Gluconobacter</i> pairing that reduced <i>P</i>. <i>expansum</i> biomass and found that <i>H</i>. <i>uvarum</i> alone is sufficient to reduce apple disease progression in vivo. We investigated possible mechanisms of <i>H</i>. <i>uvarum</i> biocontrol activity and found modest inhibition on apple puree plates, as well as a trend toward lower patulin levels at the wound site. Active biocontrol activity required live yeast, which was also effective in controlling <i>Botrytis cinerea</i> apple infections. Lastly, we explored the breadth of <i>H</i>. <i>uvarum</i> biocontrol activity with over 30 <i>H</i>. <i>uvarum</i> isolates and found consistent inhibition of <i>P</i>. <i>expansum</i> apple disease.