Phyllosphere-associated microbiota in built environment: Do they have the potential to antagonize human pathogens?

INTRODUCTION: The plant microbiota is known to protect its host against invasion by plant pathogens. Recent studies have indicated that the microbiota of indoor plants is transmitted to the local built environment where it might fulfill yet unexplored functions. A better understanding of the interplay of such microbial communities with human pathogens might provide novel cues related to natural inhibition of them. OBJECTIVE: We studied the plant microbiota of two model indoor plants, Musa acuminata and Chlorophytum comosum, and their effect on human pathogens. The main objective was to identify mechanisms by which the microbiota of indoor plants inhibits human-pathogenic bacteria. METHODS: Microbial communities and functioning were investigated using a comprehensive set of experiments and methods combining amplicon and shotgun metagenomic analyses with results from interaction assays. RESULTS: A diverse microbial community was found to be present on Musa and Chlorophytum grown in different indoor environments; the datasets comprised 1066 bacterial, 1261 fungal, and 358 archaeal ASVs. Bacterial communities were specific for each plant species, whereas fungal and archaeal communities were primarily shaped by the built environment. Sphingomonas and Bacillus were found to be prevalent components of a ubiquitous core microbiome in the two model plants; they are well-known for antagonistic activity towards plant pathogens. Interaction assays indicated that they can also antagonize opportunistic human pathogens. Moreover, the native plant microbiomes harbored a broad spectrum of biosynthetic gene clusters, and in parallel, a variety of antimicrobial resistance genes. By conducting comparative metagenomic analyses between plants and abiotic surfaces, we found that the phyllosphere microbiota harbors features that are clearly distinguishable from the surrounding abiotic surfaces. CONCLUSIONS: Naturally occurring phyllosphere bacteria can potentially act as a protective shield against opportunistic human pathogens. This knowledge and the underlying mechanisms can provide an important basis to establish a healthy microbiome in built environments.

Trade-off for survival: Microbiome response to chemical exposure combines activation of intrinsic resistances and adapted metabolic activity.

The environmental microbiota is increasingly exposed to chemical pollution. While the emergence of multi-resistant pathogens is recognized as a global challenge, our understanding of antimicrobial resistance (AMR) development from native microbiomes and the risks associated with chemical exposure is limited. By implementing a lichen asa bioindicatororganism and model for a native microbiome, we systematically examined responses towards antimicrobials (colistin, tetracycline, glyphosate, and alkylpyrazine). Despite an unexpectedly high resilience, we identified potential evolutionary consequences of chemical exposure in terms of composition and functioning of native bacterial communities. Major shifts in bacterial composition were observed due to replacement of naturally abundant taxa; e.g. Chthoniobacterales by Pseudomonadales. A general response, which comprised activation of intrinsic resistance and parallel reduction of metabolic activity at RNA and protein levels was deciphered by a multi-omics approach. Targeted analyses of key taxa based on metagenome-assembled genomes reflected these responses but also revealed diversified strategies of their players. Chemical-specific responses were also observed, e.g., glyphosate enriched bacterial r-strategists and activated distinct ARGs. Our work demonstrates that the high resilience of the native microbiota toward antimicrobial exposure is not only explained by the presence of antibiotic resistance genes but also adapted metabolic activity as a trade-off for survival. Moreover, our results highlight the importance of native microbiomes as important but so far neglected AMR reservoirs. We expect that this phenomenon is representative for a wide range of environmental microbiota exposed to chemicals that potentially contribute to the emergence of antibiotic-resistant bacteria from natural environments.