Evidence of ESBL plasmid transfer and selective persistence of multiple host-associated Escherichia coli isolates in a chicken cecal fermentation model.

IF 3.7 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
J Leng, M Ferrandis-Vila, R Oldenkamp, J W Mehat, A S Fivian-Hughes, S Kumar Tiwari, B Van der Putten, V Trung Nguyen, A Bethe, J Clark, P Singh, T Semmler, S Schwarz, J Alvarez, N T Hoa, M Bootsma, C Menge, C Berens, C Schultsz, J M Ritchie, R M La Ragione
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引用次数: 0

Abstract

The guts of animals and humans harbor diverse microbial communities that are regularly exposed to bacteria originating from food, water, and their surroundings. Species such as Escherichia coli are adept at colonizing multiple hosts, along with surviving in the environment. By encoding pathogenic traits and transmissible forms of antimicrobial resistance (AMR), E. coli can also pose a zoonotic risk. Our understanding of the factors that govern host residency is limited. Here, we used a chicken cecal fermentation model to study survival and the AMR transfer potential of 17 host-associated extended-spectrum β-lactamase (ESBL)-producing E. coli isolates. Vessels containing chicken cecal contents were stabilized for 4 days before the addition of a cocktail comprising ESBL-producing E. coli obtained from human, cattle, pig, and chicken hosts. Consecutive sampling showed that pig and cattle-associated isolates persisted in most vessels, although the recovery of all isolates declined over time. Increasing the inoculum dose or adding ceftiofur helped to stabilize populations of ESBL E. coli within the vessels, although this did not result in outgrowth of resistant populations in all vessels. Sequencing revealed that most new ESBL-producing E. coli recovered during the study acquired a blaCTX-M-1 plasmid from a single ESBL E. coli included in the cocktail that lacked host-specific traits (generalist). Our data highlight that isolate-specific differences in the E. coli genome composition likely explain the persistence of specific clones and efficiency of plasmid transfer, both of which could impact the spread of AMR in complex communities.IMPORTANCEThere are few insights into how host-associated Escherichia coli behave within the gut environment of other hosts. E. coli isolates that are immigrants to the gastrointestinal system of humans and animals have the potential to transfer their resistance to other native bacteria. A better understanding of this process is needed to assess how the gastrointestinal environment could serve as a reservoir and a melting pot of new, multidrug-resistant E. coli isolates.

鸡盲肠发酵模型中ESBL质粒转移和多种宿主相关大肠杆菌分离株选择性持久性的证据。
动物和人类的肠道中有多种微生物群落,它们经常暴露于来自食物、水及其周围环境的细菌中。像大肠杆菌这样的物种擅长于在多个宿主中定居,并在环境中生存。通过编码致病性性状和抗微生物药物耐药性(AMR)的传播形式,大肠杆菌也可能造成人畜共患风险。我们对决定寄主居住的因素的了解是有限的。本研究采用鸡盲肠发酵模型,研究了17株产生宿主相关广谱β-内酰胺酶(ESBL)的大肠杆菌的存活和AMR转移潜力。在加入含有从人、牛、猪和鸡宿主中获得的产esbl大肠杆菌的鸡尾酒之前,将含有鸡盲肠内容物的容器稳定4天。连续取样表明,尽管所有分离株的回收率随着时间的推移而下降,但大多数血管中仍存在与猪和牛相关的分离株。增加接种剂量或添加头孢替弗有助于稳定血管内的ESBL大肠杆菌种群,尽管这并不能导致所有血管中都生长出耐药种群。测序显示,在研究中恢复的大多数新的产生ESBL的大肠杆菌获得了blaCTX-M-1质粒,这些质粒来自鸡尾酒中包含的单个ESBL大肠杆菌,缺乏宿主特异性特征(多能型)。我们的数据强调,大肠杆菌基因组组成的分离特异性差异可能解释了特定克隆的持久性和质粒转移的效率,这两者都可能影响AMR在复杂群落中的传播。关于宿主相关的大肠杆菌如何在其他宿主的肠道环境中表现的见解很少。大肠杆菌分离株是人类和动物胃肠道系统的移民,有可能将其耐药性转移给其他本地细菌。需要更好地了解这一过程,以评估胃肠道环境如何成为新的耐多药大肠杆菌分离株的储存库和大熔炉。
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来源期刊
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
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