Abstract
BackgroundAntimicrobial resistance (AMR) is a major threat to public health. Microorganisms equipped with AMR genes are suggested to have partially emerged from natural habitats; however, this hypothesis remains inconclusive so far. To understand the consequences of the introduction of exogenic antimicrobials into natural environments, we exposed lichen thalli of Peltigera polydactylon, which represent defined, highly diverse miniature ecosystems, to clinical (colistin, tetracycline), and non-clinical (glyphosate, alkylpyrazine) antimicrobials. We studied microbiome responses by analysing DNA- and RNA-based amplicon libraries and metagenomic datasets.ResultsThe analyzed samples consisted of the thallus-forming fungus that is associated with cyanobacteria as well as other diverse and abundant bacterial communities (up to 108 16S rRNA gene copies ng-1 DNA) dominated by Alphaproteobacteria and Bacteroidetes. Moreover, the natural resistome of this meta-community encompassed 728 AMR genes spanning 30 antimicrobial classes. Following 10 days of exposure to the selected antimicrobials at four different concentrations (full therapeutic dosage and a gradient of sub-therapeutic dosages), we observed statistically significant, antimicrobial-specific shifts in the structure and function but not in bacterial abundances within the microbiota. We observed a relatively lower response after the exposure to the non-clinical compared to the clinical antimicrobial compounds. Furthermore, we observed specific bacterial responders, e.g., Pseudomonas and Burkholderia to clinical antimicrobials. Interestingly, the main positive responders naturally occur in low proportions in the lichen holobiont. Moreover, metagenomic recovery of the responders’ genomes suggested that they are all naturally equipped with specific genetic repertoires that allow them to thrive and bloom when exposed to antimicrobials. Of the responders, Sphingomonas, Pseudomonas, and Methylobacterium showed the highest potential.ConclusionsAntimicrobial exposure resulted in a microbial dysbiosis due to a bloom of naturally low abundant taxa (positive responders) with specific AMR features. Overall, this study provides mechanistic insights into community-level responses of a native microbiota to antimicrobials and suggests novel strategies for AMR prediction and management.5PcaefkxD7UtmCn8b7Sc8EVideo
Highlights
Antimicrobial resistance (AMR) is an increasingly serious threat to global public health [1]
We studied bacterial community responses in the ‘many-fruited pelt lichen’ Peltigera polydactylon (Neck.) Hoffm. during exposure to a full therapeutic dosage and a gradient of sub-therapeutic dosages of four antimicrobials by deoxyribonucleic acid (DNA)- and ribonucleic acid (RNA)-based amplicon sequencing along with a metagenomic dataset analyses
We addressed the following questions: (i) Is there a specific microbial shift induced by antimicrobial exposure? (ii) Which taxa respond to antimicrobial exposure? And (iii) which genetic reservoir allows positive responders to thrive under antimicrobial exposure? Overall, this study provides key insights on how antimicrobial exposure shapes microbial communities in their natural environments and provides insights into the potential consequences of modern antimicrobial overuse
Summary
Antimicrobial resistance (AMR) is an increasingly serious threat to global public health [1]. New resistance mechanisms are emerging and spreading globally, which reduces our means to treat common infectious diseases and increasingly results in prolonged illness, disability, and death [1]. Current research suggests that the unexplored diversity of resistance mechanisms in environmental bacteria is a risk factor for the human population, and clinical pathogens that are equipped with AMR [2]. Natural environments are described as the origins and reservoirs of antimicrobial resistance genes (ARGs) [3]. To fully understand the evolution, emergence and spread of antimicrobial resistance, it is crucial to study natural systems that are not disturbed by anthropogenic factors. Antimicrobial resistance (AMR) is a major threat to public health. We studied microbiome responses by analysing DNA- and RNA-based amplicon libraries and metagenomic datasets
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