Occurrence and Transmission of blaNDM-Carrying Enterobacteriaceae from Geese and the Surrounding Environment on a Commercial Goose Farm

Occurrence and Transmission of blaNDM-Carrying Enterobacteriaceae from Geese and the Surrounding Environment on a Commercial Goose Farm
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商业养鹅场鹅及其周围环境中携带 bla(NDM) 肠杆菌科细菌的发生和传播

DOI:
10.1128/aem.00087-21
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发表时间:
2021-05-01
影响因子:
4.4
通讯作者:
Fang, Liang-Xing
Fang, Liang-Xing
中科院分区:
生物学2区
文献类型:
--
作者:
Cen, Dao-Ji;Sun, Ruan-Yang;Fang, Liang-Xing

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我们调查了产NDM肠杆菌科在中国南方某鹅场鹅粪便和环境样品中的流行和传播情况。将样品在补充有美罗培南的麦康凯琼脂平板上培养。检查单个菌落的bla(NDM),并基于来自Illumina和Oxford Nanopore Technologies(ONT)平台的全基因组测序(WGS)数据表征bla(NDM)阳性细菌。在分析的117份样本中,新德里金属β-内酰胺酶(NDM)阳性肠杆菌科的携带率在鹅、无生命环境(污水、土壤、饲料和灰尘)和小鼠样本中分别为47.1%、18%和50%。在44株bla(NDM)阳性肠杆菌科中发现了两种变异株(bla(NDM-1)和bla(NDM-5),分别为4株和40株);这些变异株属于8个种,大肠埃希菌最常见(50%)。WGS分析表明,bla(NDM)与多种抗生素耐药基因(ARG)共存。种群结构分析表明,大部分E.大肠杆菌和肠杆菌属的分离株具有高度异质性,而大多数柠檬酸杆菌属和斯氏假单胞菌的分离株具有极高的遗传相似性。此外,bla(NDM-5)阳性的ST 4358/ST 48 E.大肠杆菌分离株被发现在鹅和环境之间克隆传播,并且与中国鸭、农场环境和人类中报道的分离株在遗传上高度相似。质粒分析表明,IncX 3 pHNYX 644 -1样质粒(n= 40)和不可分型的pM2-1样质粒(n = 4)介导bla(NDM)传播。pM2-1样质粒具有多种ARG,包括bla(NDM-1)、砷和汞抗性操纵子以及麦芽糖操纵子。我们的研究结果显示,鹅场是一个水库的NDM阳性肠杆菌。野生小鼠的bla(NDM)污染和新的pM2-1-like质粒可能增加了bla(NDM)及其相关耐药基因传播的风险。重要性碳青霉烯类耐药菌,特别是产NDM的肠杆菌科细菌,已成为全球公众的巨大威胁。这些细菌不仅在医院和社区环境中发现,而且在食用动物生产链中也发现,这些生产链被认为是产生NDM的肠杆菌科的储存库。然而,在水禽养殖场传播的NDM生产细菌一直没有得到很好的探索。我们的研究表明,bla(NDM)携带质粒的水平传播和bla(NDM)阳性肠杆菌科细菌的部分克隆传播有助于bla(NDM)在鹅场生态系统中的广泛污染,包括小鼠。此外,我们发现了一种新的和可转移的bla(NDM-1)携带多药耐药(MDR)质粒,具有多个环境适应相关基因。本研究的结果有助于更好地了解农场生态系统中不同生态位中携带bla(NDM)的肠杆菌科细菌的流行和传播。
We investigated the prevalence and transmission of NDM-producing Enterobacteriaceae in fecal samples of geese and environmental samples from a goose farm in southern China. The samples were cultivated on MacConkey agar plates supplemented with meropenem. Individual colonies were examined for bla(NDM), and bla(NDM)-positive bacteria were characterized based on whole- genome sequencing (WGS) data from the Illumina and Oxford Nanopore Technologies (ONT) platforms. Of 117 samples analyzed, the carriage rates for New Delhi metallo-beta-lactamase (NDM)-positive Enterobacteriaceae were 47.1, 18, and 50% in geese, inanimate environments (sewage, soil, fodder, and dust), and mouse samples, respectively. Two variants (bla(NDM-1) and bla(NDM-5), in 4 and 40 isolates, respectively) were found among 44 bla(NDM)-positive Enterobacteriaceae; these variants belonged to eight species, and Escherichia coli was the most prevalent ( 50%). WGS analysis revealed that bla(NDM) coexisted with diverse antibiotic resistance genes (ARGs). Population structure analysis showed that most E. coli and Enterobacter sp. isolates were highly heterogeneous, while most Citrobacter sp. and P. stuartii isolates possessed extremely high genetic similarities. In addition, bla(NDM-5)-positive ST4358/ST48 E. coli isolates were found to be clonally spread between geese and the environment and were highly genetically similar to those reported from ducks, farm environments, and humans in China. Plasmid analysis indicated that IncX3 pHNYX644-1-like ( n= 40) and untypeable pM2-1-like plasmids (n = 4) mediated bla(NDM) spread. pM2-1-like plasmids possessed diverse ARGs, including bla(NDM-1), the arsenical and mercury resistance operons, and the maltose operon. Our findings revealed that the goose farm is a reservoir for NDM-positive Enterobacteriaceae. The bla(NDM) contamination of wild mice and the novel pM2-1-like plasmid described here likely adds to the risk for dissemination of bla(NDM) and associated resistance genes.IMPORTANCE Carbapenem-resistant bacteria, in particular NDM-producing Enterobacteriaceae, have become a great threat to global public. These bacteria have been found not only in hospital and community environments but also among food animal production chains, which are recognized as reservoirs for NDM-producing Enterobacteriaceae. However, the dissemination of NDM-producing bacteria in waterfowl farms has been less well explored. Our study demonstrates that the horizontal spread of bla(NDM)-carrying plasmids and the partial clonal spread of bla(NDM)-positive Enterobacteriaceae contribute to the widespread contamination of bla(NDM) in the goose farm ecosystem, including mice. Furthermore, we found a novel and transferable bla(NDM-1)-carrying multidrug resistance (MDR) plasmid that possessed multiple environmental adaptation-related genes. The outcomes of this study contribute to a better understanding of the prevalence and transmission of bla(NDM)-carrying Enterobacteriaceae among diverse niches in the farm ecosystem.