Aeromonas spp. from hospital sewage act as a reservoir of genes resistant to last-line antibiotics

Yuchen Wu; Ning Dong; Chang Cai; Yu Zeng; Jiayue Lu; Congcong Liu; Hanyu Wang; Yanyan Zhang; Ling Huang; Weishuai Zhai; Dongyan Shao; Ruichao Li; Dejun Liu; Sheng Chen; Rong Zhang

doi:10.1016/j.drup.2023.100925

Aeromonas spp. from hospital sewage act as a reservoir of genes resistant to last-line antibiotics

Drug Resist Updat. 2023 Mar:67:100925. doi: 10.1016/j.drup.2023.100925. Epub 2023 Jan 11.

Authors

Yuchen Wu¹, Ning Dong², Chang Cai³, Yu Zeng⁴, Jiayue Lu¹, Congcong Liu¹, Hanyu Wang⁵, Yanyan Zhang¹, Ling Huang⁶, Weishuai Zhai⁷, Dongyan Shao⁷, Ruichao Li⁸, Dejun Liu⁷, Sheng Chen⁹, Rong Zhang¹⁰

Affiliations

¹ Department of Clinical Laboratory, Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China.
² Department of Medical Microbiology, School of Biology and Basic Medical Science, Medical College of Soochow University, Suzhou, China; Suzhou Key Laboratory of Pathogen Bioscience and Anti-infective Medicine, Soochow University, Suzhou, China.
³ China Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology, Zhejiang Agricultural and Forestry University, Hangzhou, China.
⁴ Department of Laboratory Medicine, Shenzhen University General Hospital, Shenzhen, China.
⁵ New Jersey Institute of Technology, NJ, United States.
⁶ Department of Clinical Laboratory, The Women's and Children's Hospital of Linping District, Hangzhou, China.
⁷ College of Veterinary Medicine, China Agricultural University, Beijing, China.
⁸ Jiangsu Co-Innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, College of Veterinary Medicine, Yangzhou University, Jiangsu, China.
⁹ Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong Special Administrative Region, China. Electronic address: shechen@cityu.edu.hk.
¹⁰ Department of Clinical Laboratory, Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China. Electronic address: zhang-rong@zju.edu.cn.

PMID: 36696835
DOI: 10.1016/j.drup.2023.100925

Abstract

Background: Aeromonas species are opportunistic pathogens distributed widely in the ecosystem. They are known to be capable of acquiring antibiotic resistance genes, including those encoding proteins against last-line antibiotics, such as the tmexCD-toprJ, mcr and carbapenemase genes. We investigated the genomic and phenotypic characteristics of tmexCD-toprJ-positive Aeromonas strains collected from human, animals, and water samples, particularly those from hospital wastewater in China.

Methods: Samples were collected from living animals, meat, water and human. Aeromonas strains in these samples were isolated in selective media. Antimicrobial resistance profiles of all Aeromonas strains were tested by the broth microdilution method. The presence of tmexCD-toprJ was verified by polymerase chain reaction (PCR). All tmexCD-toprJ-positive (n = 36) and selected tmexCD-toprJ-negative (n = 18) Aeromonas strains were subjected to whole genome sequencing. Carriage of antimicrobial resistance genes, the genetic environment of tmexCD-toprJ and genetic diversity of tmexCD-toprJ-positive Aeromonas strains were determined by bioinformatics analysis. Phylogenetic tree of the Aeromonas strains was built by using the Harvest Suite.

Findings: Among the 636 Aeromonas strains isolated from different sources, 36 were positive for tmexCD-toprJ, with the highest prevalence of tmexCD-toprJ being found in fishes (8.8%, 95 CI% 3.6-17.2%), followed by hospital wastewater (6.5%, 95 CI% 4.3-9.3%), river water (2.0%, 0.1-10.9) and duck (1.2%, 95 CI% 3.6-17.2%). All tmexCD-toprJ-positive Aeromonas strains carried multiple antimicrobial resistance genes and exhibited resistance to different classes of antibiotics. Co-existence of tmexCD-toprJ, mcr and bla_KPC-2 were identified in 21 strains. The tmexCD-toprJ-positive Aeromonas strains were genetically diverse and found to belong to four different species that could be clustered into three major lineages. The tmexCD-toprJ gene clusters were predominantly located in the chromosome (35/36) of Aeromonas spp., with only one strain carrying the plasmid-borne tmexCD-toprJ cluster. The tmexCD-toprJ genes were associated with seven different types of genetic environments, each of which carried distinct types of mobile elements that may be responsible for mediating transmission of this gene cluster.

Keywords: Aeromonas; Antimicrobial resistance; Last line antibiotics; TmexCD-toprJ.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Aeromonas* / genetics
Animals
Anti-Bacterial Agents / pharmacology
Drug Resistance, Bacterial / genetics
Ecosystem
Humans
Microbial Sensitivity Tests
Phylogeny
Sewage
Wastewater
Water

Substances

Anti-Bacterial Agents
Sewage
Wastewater
Water