Horizontal plasmid transfer promotes antibiotic resistance in selected bacteria in Chinese frog farms

Mei Zhuang; Waner Yan; Yifei Xiong; Zhilin Wu; Yuping Cao; Edmond Sanganyado; Bupe A. Siame; Liang Chen; Yechezkel Kashi; Ka Yin Leung

Environment International (Aug 2024)

Horizontal plasmid transfer promotes antibiotic resistance in selected bacteria in Chinese frog farms

Mei Zhuang,
Waner Yan,
Yifei Xiong,
Zhilin Wu,
Yuping Cao,
Edmond Sanganyado,
Bupe A. Siame,
Liang Chen,
Yechezkel Kashi,
Ka Yin Leung

Affiliations

Mei Zhuang: Faculty of Biotechnology and Food Engineering, Technion-Israel Institute of Technology, Haifa, Israel; Department of Biotechnology and Food Engineering Program, Guangdong Technion-Israel Institute of Technology, Shantou 515063, China
Waner Yan: Department of Microbiology and Molecular Genetics, The Hebrew University of Jerusalem, POB 12272, Jerusalem 91120, Israel
Yifei Xiong: Department of Microbiology and Molecular Genetics, The Hebrew University of Jerusalem, POB 12272, Jerusalem 91120, Israel
Zhilin Wu: Department of Microbiology and Molecular Genetics, The Hebrew University of Jerusalem, POB 12272, Jerusalem 91120, Israel
Yuping Cao: Faculty of Biotechnology and Food Engineering, Technion-Israel Institute of Technology, Haifa, Israel; Department of Biotechnology and Food Engineering Program, Guangdong Technion-Israel Institute of Technology, Shantou 515063, China
Edmond Sanganyado: Department of Applied Sciences, Northumbria University, Newcastle Upon Tyne NE1 8ST, UK
Bupe A. Siame: Department of Biology, Trinity Western University, Langley, British Columbia V2Y 1Y1, Canada
Liang Chen: Department of Computer Science, College of Mathematics and Computer, Shantou University, Shantou 515063, China; Corresponding authors.
Yechezkel Kashi: Faculty of Biotechnology and Food Engineering, Technion-Israel Institute of Technology, Haifa, Israel
Ka Yin Leung: Faculty of Biotechnology and Food Engineering, Technion-Israel Institute of Technology, Haifa, Israel; Department of Biotechnology and Food Engineering Program, Guangdong Technion-Israel Institute of Technology, Shantou 515063, China; Corresponding authors.

Journal volume & issue: Vol. 190
p. 108905

Abstract

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The emergence and dissemination of antibiotic resistance genes (ARGs) in the ecosystem are global public health concerns. One Health emphasizes the interconnectivity between different habitats and seeks to optimize animal, human, and environmental health. However, information on the dissemination of antibiotic resistance genes (ARGs) within complex microbiomes in natural habitats is scarce. We investigated the prevalence of antibiotic resistant bacteria (ARB) and the spread of ARGs in intensive bullfrog (Rana catesbeiana) farms in the Shantou area of China. Antibiotic susceptibilities of 361 strains, combined with microbiome analyses, revealed Escherichia coli, Edwardsiella tarda, Citrobacter and Klebsiella sp. as prevalent multidrug resistant bacteria on these farms. Whole genome sequencing of 95 ARB identified 250 large plasmids that harbored a wide range of ARGs. Plasmid sequences and sediment metagenomes revealed an abundance of tetA, sul1, and aph(3″)-Ib ARGs. Notably, antibiotic resistance (against 15 antibiotics) highly correlated with plasmid-borne rather than chromosome-borne ARGs. Based on sequence similarities, most plasmids (62%) fell into 32 distinct groups, indicating a potential for horizontal plasmid transfer (HPT) within the frog farm microbiome. HPT was confirmed in inter- and intra-species conjugation experiments. Furthermore, identical mobile ARGs, flanked by mobile genetic elements (MGEs), were found in different locations on the same plasmid, or on different plasmids residing in the same or different hosts. Our results suggest a synergy between MGEs and HPT to facilitate ARGs dissemination in frog farms. Mining public databases retrieved similar plasmids from different bacterial species found in other environmental niches globally. Our findings underscore the importance of HPT in mediating the spread of ARGs in frog farms and other microbiomes of the ecosystem.

Published in Environment International

ISSN: 0160-4120 (Print)
Publisher: Elsevier
Country of publisher: United Kingdom
LCC subjects: Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/environment-international

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