One health genomic insights into the host-specific evolution and cross-host transmission of Staphylococcus aureus in animal farm environments, food of animal origin, and humans

Yu Pan; Lin Chen; Lingxuan Zhang; Guihua Li; Jiaxiong Zeng; Jianxin Hu; Weiqi Liu; Yafei Li; Zhenling Zeng

doi:10.1016/j.ijantimicag.2023.106932

One health genomic insights into the host-specific evolution and cross-host transmission of Staphylococcus aureus in animal farm environments, food of animal origin, and humans

Int J Antimicrob Agents. 2023 Oct;62(4):106932. doi: 10.1016/j.ijantimicag.2023.106932. Epub 2023 Jul 24.

Authors

Yu Pan¹, Lin Chen¹, Lingxuan Zhang², Guihua Li³, Jiaxiong Zeng⁴, Jianxin Hu¹, Weiqi Liu³, Yafei Li⁵, Zhenling Zeng⁶

Affiliations

¹ College of Veterinary Medicine, National Risk Assessment Laboratory for Antimicrobial Resistant of Microorganisms in Animals, Guangdong Provincial Key Laboratory of Veterinary Pharmaceutics Development and Safety Evaluation, South China Agricultural University, Guangzhou, China; Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China.
² Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China.
³ College of Veterinary Medicine, National Risk Assessment Laboratory for Antimicrobial Resistant of Microorganisms in Animals, Guangdong Provincial Key Laboratory of Veterinary Pharmaceutics Development and Safety Evaluation, South China Agricultural University, Guangzhou, China.
⁴ School of Environmental Science and Engineering, Sun Yat-sen University, Guangzhou, China.
⁵ Institute of Quality Standard and Monitoring Technology for Agro-products of Guangdong Academy of Agricultural Sciences, Guangzhou, China. Electronic address: yafei.lee@163.com.
⁶ College of Veterinary Medicine, National Risk Assessment Laboratory for Antimicrobial Resistant of Microorganisms in Animals, Guangdong Provincial Key Laboratory of Veterinary Pharmaceutics Development and Safety Evaluation, South China Agricultural University, Guangzhou, China; Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou, China. Electronic address: zlzeng@scau.edu.cn.

PMID: 37495058
DOI: 10.1016/j.ijantimicag.2023.106932

Abstract

Objectives: Staphylococcus aureus is an opportunistic pathogen that is considered a high priority for research. However, comparative studies of S. aureus strains from different environments and hosts are still lacking.

Methods: Here, we performed a high-resolution bioinformatics analysis of 576 S. aureus genomes isolated from livestock, farm environments, farm workers, animal-origin food, and humans.

Results: The S. aureus isolates showed high diversity in genetic lineages and demonstrated host specialization and multi-host range in the population phylogeny. Recent transmission events, historical divergences, and frequent host switching in specific sequence types (STs) and through the food chain and animal farm mediums were observed. Frequent gene transfer may quickly give rise to new fitness to colonize their host or switch to other hosts, even in isolates with the closest vertical evolutionary history. The large multi-host-shared antibiotic resistance gene (ARG) pool was the major factor shaping antibiotic resistance in S. aureus isolates. We revealed the genetic backgrounds of mec, cfr, and optrA, which could be spread among isolates from different species, hosts, and environments.

Conclusion: Overall, our findings provide One Health genomic insights into the evolution, transmission, gene content characteristics, and antibiotic resistance profiles of S. aureus from different hosts, suggesting that, despite well-formed host specificity during the evolution of S. aureus, the ever-expanding host range and the cross-hosts/niches transmission (at both the strain and genetic level) may be facilitated by diverse bacterial vehicles (e.g., food chain, farm environments, and workers), which will lead to emerging antibiotic resistance consequences and threaten public health and food safety.

Keywords: Antibiotic resistance; One Health surveillance; Public health; Staphylococcus aureus; Whole-genome sequencing.