Abstract

BackgroundArugula is a traditional medicinal plant and popular leafy green today. It is mainly consumed raw in the Western cuisine and known to contain various bioactive secondary metabolites. However, arugula has been also associated with high-profile outbreaks causing severe food-borne human diseases. A multiphasic approach integrating data from metagenomics, amplicon sequencing, and arugula-derived bacterial cultures was employed to understand the specificity of the indigenous microbiome and resistome of the edible plant parts.ResultsOur results indicate that arugula is colonized by a diverse, plant habitat-specific microbiota. The indigenous phyllosphere bacterial community was shown to be dominated by Enterobacteriaceae, which are well-equipped with various antibiotic resistances. Unexpectedly, the prevalence of specific resistance mechanisms targeting therapeutic antibiotics (fluoroquinolone, chloramphenicol, phenicol, macrolide, aminocoumarin) was only surpassed by efflux pump assignments.ConclusionsEnterobacteria, being core microbiome members of arugula, have a substantial implication in the overall resistome. Detailed insights into the natural occurrence of antibiotic resistances in arugula-associated microorganisms showed that the plant is a hotspot for distinctive defense mechanisms. The specific functioning of microorganisms in this unusual ecosystem provides a unique model to study antibiotic resistances in an ecological context.

Highlights

  • Arugula is a traditional medicinal plant and popular leafy green today

  • The arugula microbiome and the community structure of the enterobacterial fraction Assembly-based community structure analyses of habitat-specific metagenomes showed a high proportion of contigs assigned to Proteobacteria, which were relatively evenly distributed among the analyzed habitats

  • Alignments showed that the habitats harbored a similar enterobacterial diversity; there were substantial variations in abundances between the metagenomes

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Summary

Introduction

Arugula is a traditional medicinal plant and popular leafy green today. It is mainly consumed raw in the Western cuisine and known to contain various bioactive secondary metabolites. All members of the Brassicaceae plant family characterized far have shown an extraordinary degree of specificity in their associated microbiota [6, 7, 65]. They are known for a bacteria-dominated composition of the microbiome, as they do not harbor a typical mycorrhiza [30, 54]. The effective defense mechanisms of the plant are based on a unique composition of antimicrobial secondary metabolites, including glucosinolates [42, 52] Their resulting degradation products (isothiocyanates) have received scientific interest, as they might be involved in cancer prevention [31]. Our hypothesis was that arugula would be associated with a highly specialized microbiota, due to metabolites it produces, which were expected to be highly different from salad species from the Asteraceae family, which have been well studied previously [18, 53]

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