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

Abstract

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.

Bitter friends are not always toxic: The loss of acetic acid bacteria and the absence of Komagataeibacter in the gut microbiota of the polyphagous fly Anastrepha ludens could inhibit its development in Psidium guajava in contrast to A. striata and A. fraterculus that flourish in this host

“…We fully recognize, that ideally, we should have compared the two types of pulp, totally clean, uninfested pulp, and pulp in the vicinity of the feeding larvae. However, based on literature reports ( Drobya and Wisniewskib, 2018 ; Huang et al, 2020 ; Zhang et al, 2021 ; Malacrinò et al, 2022 ; Wassermann et al, 2022 ), we knew that pulp from an undamaged/intact (i.e., insect, pathogen, bird damage) fruit, contain a very different microbial profile (endophytic bacteria and fungi), and once a wound occurs, the microbiota profile changes rapidly. In our study we found components of the gut microbiotas of some of the fruit fly species studied in the pulp, such as the endosymbiont Wolbachia , which suggests that the larvae modify the pulp microbiota as Wolbachia is not a fruit endophyte.…”

Report of the Scientific Committee of the Spanish Agency for Food Safety and Nutrition (AESAN) on the effects of climate change on food allergy

“…Furthermore, arable areas are usually located at a long distance from the consumer, which requires the transport of food, in special containers, with chemical preserving agents and with special treatments to increase the storage time or the attractive appearance (for example, the waxing of revista del comité científico nº 38 AESAN Scientific Committee: Effects of climate change on food allergy apples). All these treatments cause a reduction in the biodiversity of the food microbiome, which can affect the microbiome of the human intestine, leading to a profound impact on the intestinal barrier (Wassermann et al, 2022), which favors the appearance of food allergies. Overall, a lower biodiversity of the environment, the soil, the plants, the food and, possibly, less social contact, can affect the microbiome of the skin and the intestine and, therefore, to the immune balance of people, resulting in an allergic sensitization (Haahtela, 2013) (Haahtela et al, 2021) (Borbet et al, 2022).…”

The One Health approach for allergic diseases and asthma

“…[76][77][78][79][80] The growing conditions (organic vs. conventional), transport of food over long distances, and special treatment to increase storage time or attractiveness (e.g., waxing of apples) result in changed or lower biodiversity of the microbiome on the food, potentially also impacting the microbiome in the gut, together with a profound impact on the gut barrier. 81 Another outcome of poor diversity of soil and environment may include loss of binding partners for specific proteins like lipocalins which turn from tolerogens (proteins with their binding partners like iron-siderophores, vitamins A and D, or zinc) into allergens (empty proteins). [82][83][84][85] In addition to changed microbiome and ligand-binding for carrier proteins, reduced biodiversity diminishes contact with stimulants for innate responses (e.g.…”

“…Resulting nutrient deficiencies, obesity, and a changed microbial composition lead directly or indirectly to immune‐related noncommunicable diseases 76–80 . The growing conditions (organic vs. conventional), transport of food over long distances, and special treatment to increase storage time or attractiveness (e.g., waxing of apples) result in changed or lower biodiversity of the microbiome on the food, potentially also impacting the microbiome in the gut, together with a profound impact on the gut barrier 81 …”