Inhalable antibiotic resistomes emitted from hospitals: metagenomic insights into bacterial hosts, clinical relevance, and environmental risks

Background: Threats of antimicrobial resistance (AMR) to human health are on the rise worldwide. Airborne fine particulate matter (PM2.5), especially those emitted from hospitals, could serve as a substantial yet lesser-known environmental medium of inhalable antibiotic resistomes. A genome-centric understanding of the hosting bacterial taxa, mobility potential, and consequent risks of the resistomes is needed to reveal the health relevance of PM2.5-associated AMR from clinical settings. Results: Compared to urban ambient air PM2.5, the hospital samples harbored nearly twice the abundance of antibiotic resistantance genes (ARGs, similar to 0.2 log(10) (ARGs/16S rRNA gene)) in the summer and winter sampled. The profiled resistome was closely correlated with the human-source-influenced (similar to 30% of the contribution) bacterial community (Procrustes test, P < 0.001), reflecting the potential antibiotic-resistant bacteria (PARB), such as the human commensals Staphylococcus spp. and Corynebacterium spp. Despite the reduced abundance and diversity of the assembled metagenomes from summer to winter, the high horizontal transfer potential of ARGs, such as the clinically relevant bla(OXA) and bacA, in the human virulent PARB remained unaffected in the hospital air PM samples. The occurring patterns of beta-lactam resistance genes and their hosting genomes in the studied hospital-emitting PM(2.5 )were closely related to the in-ward beta-lactam-resistant infections (SEM, std = 0.62, P < 0.01). Featured with more abundant potentially virulent PARB (2.89 genome copies/m(3)-air), the hospital samples had significantly higher resistome risk index scores than the urban ambient air samples, indicating that daily human exposure to virulent PARB via the inhalation of PM(2.5 )was ten times greater than from the ingestion of drinking water. Conclusions: The significance of AMR in the studied hospital-emitting PM2.5 was highlighted by the greater abundance of ARGs, the prevalence of potentially virulent PARB, and the close association with hospital in-ward beta-lactam infections. A larger-scale multi-source comparison of genome-resolved antibiotic resistomes is needed to provide a more holistic understanding to evaluate the importance of airborne AMR from the One-Health perspective.

Automated summary

The study found that airborne fine particulate matter (PM2.5) emitted from hospitals contains a higher abundance of antibiotic resistance genes (ARGs) compared to urban ambient air PM2.5. The ARGs are closely associated with human-source-influenced bacterial communities, indicating the presence of potential antibiotic-resistant bacteria. The transfer potential of ARGs remains high in hospital air PM samples, and is related to beta-lactam-resistant infections within the hospital. Additionally, the study reveals that the risk of exposure to potentially virulent bacteria through inhalation of PM2.5 is ten times greater than through drinking water ingestion.