Transmission of antimicrobial resistance genes from the environment to human gut is more pronounced in colorectal cancer patients than in healthy subjects

IF 23.7 Q1 MICROBIOLOGY
iMeta Pub Date : 2025-03-05 DOI:10.1002/imt2.70008
Weixin Liu, Harry C. H. Lau, Xiao Ding, Xiaole Yin, William Ka Kei Wu, Sunny Hei Wong, Joseph J. Y. Sung, Tong Zhang, Jun Yu
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Abstract

Antimicrobial resistance is a major global health concern. However, the source of gut resistome remains unsolved. We aimed to analyze the contribution of environmental antimicrobial resistance genes (ARGs) to colorectal cancer (CRC) patients. Here, we collected metagenomic data from 1,605 human stool samples (CRC = 748; healthy = 857) and 1,035 city-matched environmental samples, in which 110 CRC, 112 healthy, and 56 environmental samples were newly collected. Compared to healthy subjects, CRC patients had significantly higher ARG burden (p < 0.01) with increased levels of multidrug-resistant ARGs. Gut ARGs in CRC also had a closer similarity to environmental ARGs (p < 0.001). By comparing environmental and gut ARGs, 28 environmental ARGs were identified as CRC-specific ARGs, including SUL2 and MEXE, which were not identified in healthy subjects. Meanwhile, more mobile ARGs (mARGs) from the environment were observed in CRC patients compared to healthy subjects (p < 0.05). The hosts of mARGs were mainly pathogenic bacteria (e.g., Escherichia coli (E. coli) and Clostridium symbiosum (C. symbiosum)). Compared to healthy subjects, CRC patients showed elevated horizontal gene transfer efficiency from the environment to gut. Consistently, the abundance of pathobionts carrying specific mARGs (e.g., E. coli-SUL2 and C. symbiosum-SUL2) were significantly increased in CRC patients compared to healthy subjects (p < 0.05). We thus reveal a route of ARG dissemination from the environment into the gut of CRC patients.

Abstract Image

抗生素耐药基因从环境到人类肠道的传播在结直肠癌患者中比在健康受试者中更为明显
抗微生物药物耐药性是一个主要的全球卫生问题。然而,肠道抵抗组的来源仍未得到解决。我们旨在分析环境抗微生物药物耐药性基因(ARGs)在结直肠癌(CRC)患者中的作用。在这里,我们收集了1605份人类粪便样本的宏基因组数据(CRC = 748;健康= 857)和1035份城市匹配环境样本,其中CRC 110份,健康112份,环境56份。与健康受试者相比,结直肠癌患者ARG负担显著增加(p < 0.01),且多药耐药ARG水平升高。结直肠癌患者肠道ARGs与环境ARGs的相似性也更大(p < 0.001)。通过比较环境ARGs和肠道ARGs,鉴定出28种环境ARGs为crc特异性ARGs,包括SUL2和MEXE,这些ARGs在健康受试者中未被鉴定出来。同时,与健康受试者相比,CRC患者观察到更多来自环境的移动ARGs (mARGs) (p < 0.05)。mARGs的宿主以致病菌为主,如大肠杆菌(E. coli)和共生梭菌(C. symbiosum)。与健康受试者相比,结直肠癌患者从环境到肠道的水平基因转移效率更高。与健康受试者相比,CRC患者携带特定mARGs的病原菌(如大肠杆菌sul2和C.共生菌sul2)的丰度显著增加(p < 0.05)。因此,我们揭示了ARG从环境传播到结直肠癌患者肠道的途径。
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CiteScore
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