Plant resistome profiling in evolutionary old bog vegetation provides new clues to understand emergence of multi-resistance

Abstract

The expanding antibiotic resistance crisis calls for a more in depth understanding of the importance of antimicrobial resistance genes (ARGs) in pristine environments. We, therefore, studied the microbiome associated with Sphagnum moss forming the main vegetation in undomesticated, evolutionary old bog ecosystems. In our complementary analysis of culture collections, metagenomic data and a fosmid library from different geographic sites in Europe, we identified a low abundant but highly diverse pool of resistance determinants, which targets an unexpectedly broad range of 29 antibiotics including natural and synthetic compounds. This derives both, from the extraordinarily high abundance of efflux pumps (up to 96%), and the unexpectedly versatile set of ARGs underlying all major resistance mechanisms. Multi-resistance was frequently observed among bacterial isolates, e.g. in Serratia, Rouxiella, Pandoraea, Paraburkholderia and Pseudomonas. In a search for novel ARGs, we identified the new class A β-lactamase Mm3. The native Sphagnum resistome comprising a highly diversified and partially novel set of ARGs contributes to the bog ecosystem´s plasticity. Our results reinforce the ecological link between natural and clinically relevant resistomes and thereby shed light onto this link from the aspect of pristine plants. Moreover, they underline that diverse resistomes are an intrinsic characteristic of plant-associated microbial communities, they naturally harbour many resistances including genes with potential clinical relevance.

Post-translational regulation of autophagy is involved in intra-microbiome suppression of fungal pathogens

“…This might be connected to differences in sensitivity between fungi and plants. Our finding is in line with the less known role of antibiotics in the environment; they are important signaling molecules and therefore widespread in natural habitats with high microbial diversity [ 51 ]. Former studies showed mainly direct antibiosis for Streptomyces –fungi interactions [ 52 ].…”

Antimicrobial-specific response from resistance gene carriers studied in a natural, highly diverse microbiome

“…However, the same mechanisms can also serve as an essential feature of nosocomial pathogens to overcome high (toxic) antimicrobial concentrations that are found in clinical settings [59,61]. The high diversity of ARGs that was detected in the present study, reflects the natural complexity of microbial communities that are commonly associated with lichens, and have previously been shown to provide metabolic versatility that facilitates plasticity of the lichen holobiont [13,62].…”

“…Our data highlights that the natural microbiome of Peltigera comprises highly diverse and low abundant intrinsic ARGs, which provide a retrievable basis to cope with antimicrobial pressure. Similar to other relatively pristine environments, ARGs were found to be ubiquitous and to harbour a high number of different efflux pump systems [13,59,60]. In nature, ARGs fulfil various roles and are commonly involved in processes such as detoxification and molecular signalling.…”

“…A recent study by Mahnert et al [12] demonstrated that loss of microbial diversity, due to cleaning in confined environments such as intensive care units and cleanroom facilities, correlates with an increase of antimicrobial resistance features. Despite this growing body of research that links antimicrobial exposure to changes in microbial communities, the community response to antimicrobial exposure in native environments is not yet understood [13].…”

Bog ecosystems as a playground for plant–microbe coevolution: bryophytes and vascular plants harbour functionally adapted bacteria

“…Bacteria are known to be the main constituent of the bog microbiome, co-occurring and interacting with archaea, fungi and other members of the microbiome [ 8 , 12 , 13 ]. Moreover, bog ecosystems were found to be natural hotspots for a high diversity of bacterial species and antagonists [ 12 ] and microbial genes [ 11 ] and interestingly also for antibiotic resistance genes [ 4 , 11 , 14 ]. A vast majority of bog bacteria were found to engage in a plant-associated, often endophytic life style [ 4 ].…”