The microbiome and resistome of apple fruits alter in the post-harvest period

Background A detailed understanding of antimicrobial resistance trends among all human-related environments is key to combat global health threats. In food science, however, the resistome is still little considered. Here, we studied the apple microbiome and resistome from different cultivars (Royal Gala and Braeburn) and sources (freshly harvested in South Africa and exported apples in Austrian supermarkets) by metagenomic approaches, genome reconstruction and isolate sequencing. Results All fruits harbor an indigenous, versatile resistome composed of 132 antimicrobial resistance genes (ARGs) encoding for 19 different antibiotic classes. ARGs are partially of clinical relevance and plasmid-encoded; however, their abundance within the metagenomes is very low (<= 0.03%). Post-harvest, after intercontinental transport, the apple microbiome and resistome was significantly changed independently of the cultivar. In comparison to fresh apples, the post-harvest microbiome is characterized by higher abundance of Enterobacteriales, and a more diversified pool of ARGs, especially associated with multidrug resistance, as well as quinolone, rifampicin, fosfomycin and aminoglycoside resistance. The association of ARGs with metagenome-assembled genomes (MAGs) suggests resistance interconnectivity within the microbiome. Bacterial isolates of the phyla Gammaproteobacteria, Alphaproteobacteria and Actinobacteria served as representatives actively possessing multidrug resistance and ARGs were confirmed by genome sequencing. Conclusion Our results revealed intrinsic and potentially acquired antimicrobial resistance in apples and strengthen the argument that all plant microbiomes harbor diverse resistance features. Although the apple resistome appears comparatively inconspicuous, we identified storage and transport as potential risk parameters to distribute AMR globally and highlight the need for surveillance of resistance emergence along complex food chains.