Skin Microbiota of Field-Grown Processing Tomato Fruits in Relation to Alternaria Black Spot and Mycotoxin Contamination

Tomato is among the most widely cultivated vegetable crops worldwide. However, its high susceptibility to Alternaria is particularly concerning due to the ability of fungi of this genus to produce mycotoxins that pose potential health risks. Contamination of processed tomato products has been repeatedly reported in the literature, but little is known about the factors influencing contamination in field-grown processing tomatoes. In this study, we assessed the composition of the epidermal microbiota of processing tomato fruits in relation to Alternaria and mycotoxin contamination levels. Tomato crops exhibiting varying levels of contamination (based on symptom assessment, qPCR and LC-MS/MS analysis) were selected, and both healthy and diseased fruits were sampled. Our results revealed that processing tomatoes can be heavily contaminated with Alternaria mycotoxins at harvest. Visual symptoms were not reliable predictors of toxicological risk: the observed association between Stemphylium abundance and disease severity raises the hypothesis that Stemphylium may contribute to symptoms commonly attributed to Alternaria black spot. Conversely, fruits displaying atypical symptom profiles often contained high levels of Alternaria mycotoxins. Analysis of the tomato skin microbiota using 16S and ITS metabarcoding showed that fruit health status was associated with distinct microbial communities and identified several microbial modules associated with reduced disease severity and/or lower Alternaria relative abundance. Taxa belonging to the genera Wickerhamomyces, Gibellulopsis, Ectophoma, Bacillus, Liquorilactobacillus, and Enterococcus were predominantly associated with reduced disease symptoms and/or Alternaria relative abundance. These microbial groups represent promising targets for future isolation and experimental evaluation as biocontrol agents.