A global perspective on the abundance, diversity and mobility of antibiotic resistance genes in Escherichia coli

Yun Qing; Zhongai Zou; Guolian Jiang; Lingshi Qin; Kehui Liu; Zongbao Liu

doi:10.3389/fvets.2024.1442159

A global perspective on the abundance, diversity and mobility of antibiotic resistance genes in Escherichia coli

Front Vet Sci. 2024 Nov 13:11:1442159. doi: 10.3389/fvets.2024.1442159. eCollection 2024.

Authors

Yun Qing^#^{1

2

3}, Zhongai Zou^#⁴, Guolian Jiang³, Lingshi Qin³, Kehui Liu¹, Zongbao Liu^{1

2

3}

Affiliations

¹ Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, Guilin, Guangxi, China.
² Guangxi Key Laboratory of Landscape Resources Conservation and Sustainable Utilization in Lijiang River Basin, Guangxi Normal University, Guilin, Guangxi, China.
³ College of Life Sciences, Guangxi Normal University, Guilin, Guangxi, China.
⁴ College of Environment and Public Health, Xiamen Huaxia University, Xiamen, Fujian, China.

^# Contributed equally.

Abstract

Introduction: Escherichia coli (E. coli), a ubiquitous opportunistic pathogen, poses a growing threat to human health due to the increasing prevalence of antibiotic resistance. However, a comprehensive understanding of the global distribution, diversity, and transmission of antibiotic resistance genes (ARGs) in E. coli remains lacking, hindering effective strategies to combat resistance.

Methods: In this study, we analyzed 94,762 E. coli genome sequences obtained from the NCBI database using advanced bioinformatics tools. ARGs were identified by comparing sequences against a custom ARG database using BLAST. Mobile genetic element (MGE)-associated ARGs were identified by matching with ISfinder databases. Global distribution of ARGs was analyzed by clustering mobile ARG sequences with 99% genetic similarity.

Results: Our analysis revealed that 50.51% of the E. coli genome sequences contained ARGs, totaling 301,317 identified ARG sequences. These ARGs were categorized into 12 major classes and 229 subtypes. Notably, ARGs associated with multi-drug resistance (MDR), β-lactams, macrolide-lincosamide-streptogramins (MLS), tetracyclines, and aminoglycosides were particularly abundant, with the subtypes mdtK, macB, and ampC being especially prevalent. Additionally, significant differences in ARG abundance and diversity were observed across countries, with higher diversity found in high-income nations. Furthermore, 9.28% of the ARG sequences were linked to MGEs, accounting for 98.25% of all ARG subtypes. Notably, 4.20% of mobile ARGs were identified in over 20 countries, with β-lactam and aminoglycoside ARGs being the most widespread.

Discussion: This study provides a comprehensive overview of the global distribution and transmission of ARGs in E. coli. The high abundance of MDR and β-lactam-related ARGs, along with their widespread transmission across countries, highlights the urgent need for global surveillance and control measures. Furthermore, the strong association between ARGs and MGEs underscores the role of horizontal gene transfer in the spread of resistance. The observed variations in ARG diversity between countries suggest that socioeconomic factors, such as healthcare infrastructure and antibiotic usage patterns, significantly influence ARG prevalence. These findings are crucial for informing global strategies to mitigate the spread of antibiotic resistance and improve public health outcomes.

Keywords: Escherichia coli; antibiotic resistance genes; gene transfer; global perspective; mobile genetic elements.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (grant no. 32360039), the Science and Technology Base and talent Special project of Guangxi (grant no. 2022 AC21335), and the Natural Science Foundation of Xiamen, China (3502Z20227231).