TY - JOUR
T1 - Inhalable antibiotic resistomes emitted from hospitals
T2 - metagenomic insights into bacterial hosts, clinical relevance, and environmental risks
AU - Wu, Dong
AU - Jin, Ling
AU - Xie, Jiawen
AU - Liu, Hang
AU - Zhao, Jue
AU - Ye, Dan
AU - Li, Xiang dong
N1 - Funding Information:
We thank the National Natural Science Foundation of China (92043302, 42007393 and 42107457), the Research Grants Council of Hong Kong (15210618, 15203920, 25210420, and T21-705/20-N), and the University Facility on Chemical and Environmental Analysis (UCEA) at The Hong Kong Polytechnic University for supporting this study. Dr. Dong Wu expresses appreciation for the joint funding provided by the Society of Hong Kong Scholars and the China Postdoctoral Science Foundation (XJ2018030), the National Key Research and Development Program of China (2018YFC1901000), and the Shanghai Engineering Research Center of Biotransformation of Organic Solid Waste (19DZ2254400) for their support for his research.
Publisher Copyright:
© 2022, The Author(s).
PY - 2022/12
Y1 - 2022/12
N2 - 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, ~ 0.2 log10(ARGs/16S rRNA gene)) in the summer and winter sampled. The profiled resistome was closely correlated with the human-source-influenced (~ 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 blaOXA and bacA, in the human virulent PARB remained unaffected in the hospital air PM samples. The occurring patterns of β-lactam resistance genes and their hosting genomes in the studied hospital-emitting PM2.5 were closely related to the in-ward β-lactam-resistant infections (SEM, std = 0.62, P < 0.01). Featured with more abundant potentially virulent PARB (2.89 genome copies/m3-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 PM2.5 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 β-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. [MediaObject not available: see fulltext.].
AB - 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, ~ 0.2 log10(ARGs/16S rRNA gene)) in the summer and winter sampled. The profiled resistome was closely correlated with the human-source-influenced (~ 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 blaOXA and bacA, in the human virulent PARB remained unaffected in the hospital air PM samples. The occurring patterns of β-lactam resistance genes and their hosting genomes in the studied hospital-emitting PM2.5 were closely related to the in-ward β-lactam-resistant infections (SEM, std = 0.62, P < 0.01). Featured with more abundant potentially virulent PARB (2.89 genome copies/m3-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 PM2.5 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 β-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. [MediaObject not available: see fulltext.].
KW - AMR risk
KW - Antibiotic resistome
KW - ARG-hosting bacteria
KW - Healthcare-associated infection
KW - Hospital PM
UR - http://www.scopus.com/inward/record.url?scp=85123760333&partnerID=8YFLogxK
U2 - 10.1186/s40168-021-01197-5
DO - 10.1186/s40168-021-01197-5
M3 - Journal article
C2 - 35086564
AN - SCOPUS:85123760333
SN - 2049-2618
VL - 10
JO - Microbiome
JF - Microbiome
IS - 1
M1 - 19
ER -