Naturally occurring antibiotic resistances in plant microbiomes

Antibiotic-resistant bacteria are not only restricted to clinical environments, nor do they always pose an immediate danger for humans. Various environmental niches are occupied by complex microbial communities that also include members that can carry one or different antibiotic resistances.

Published in Microbiology

Naturally occurring antibiotic resistances in plant microbiomes
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BioMed Central
BioMed Central BioMed Central

Enterobacteriaceae dominate the core microbiome and contribute to the resistome of arugula (Eruca sativa Mill.) - Microbiome

Background 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. 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. Results Our 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. Conclusions Enterobacteria, 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.

The plant microbiome often harbors highly competitive microorganisms that can shield of pathogens and contribute to the host’s health. In our latest study we have focused on antibiotic resistances in a common salad plant and found that the indigenous enterobacterial community contributes to the highly interesting profile.

The fatal implications of various infections by opportunistic human pathogens were thought of as a burden of the past, especially after several generations of highly effective antibiotics were developed. With the increased occurrence of antibiotic-resistant microorganisms (mostly bacteria), this perception is changing and we are facing once again a problem that requires a long-lasting solution. 

This solution will most likely not arise from a new generation of classic antibiotics. In fact, it will require to overthink how we administer antimicrobial agents and how to avoid the natural response of microorganisms when they are attacked. The world health organization (WHO; https://www.who.int) provides frequently updated lists of microorganisms for which antibiotic treatments are urgently required. 

Interestingly, many of the bacteria that are found on these lists have close relatives that either occur in our bodies or in natural environments that we use for our food production. Often the only difference is strain-specific and only given by certain genes that can be also located on plasmids. 

Previous studies have already shown that many plant-associated bacteria have many similarities with opportunistic human pathogens, mostly due to the fact that they require similar functional repertoires for their survival (Berg et al., 2005). These findings provide the basis to study how these microorganisms are controlled in their natural environments and how this might be transferred to environments that are relevant for our health. 

These environments are not only restricted to the clinical field, but also agricultural production and the indoor environment in general. In order to further decipher the occurrence of antibiotic resistances in natural environments, we have selected a common salad plant as a model for our study that included metagenomic profiling and cultivation-based studies in order to confirm the presence of multi-resistant bacteria. 

Eruca vesicaria var. sativa (Mill.) Thell., commonly known as arugula, is a popular raw-eaten ingredient in salads due to its peppery, pungent taste. Similar to other leafy green plants, E. sativa is colonized by a vast diversity of microbes, which complement the holobiont’s functioning. 

We analyzed the structure, abundance and functioning of the plant-associated microbiota in the arugula phyllosphere, rhizosphere and the corresponding bulk soil in an integrative approach. When compared to the rhizosphere, higher proportions of Gammaproteobacteria, including Enterobacteriaceae were observed in aerial plant parts. Metagenomic profiling of the bacterial population indicated a higher prevalence of antibiotic resistances in plant-derived samples. 

We found general resistance mechanisms including various efflux pumps in the datasets, but also specific resistance mechanisms against fluoroquinolone, chloramphenicol and other antibiotics. Our overall findings suggest that antibiotic resistance is common in distinct raw-eaten plants. This provides the basis to further explore how these resistances are formed and how carriers, which are rarely pathogens in such environments, can be controlled in the future.

Berg, G., Eberl, L., and Hartmann, A. (2005). The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environmental Microbiology, 7, 1673-1685.

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    This journal hopes to integrate researchers with common scientific objectives across a broad cross-section of sub-disciplines within microbial ecology. It covers studies of microbiomes colonizing humans, animals, plants or the environment, both built and natural or manipulated, as in agriculture.

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