Differential Overlap in Human and Animal Fecal Microbiomes and Resistomes in Rural versus Urban Bangladesh
Differential Overlap in Human and Animal Fecal Microbiomes and Resistomes in Rural versus Urban Bangladesh
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DOI：
10.1128/aem.00759-22
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发表时间：
2021-05
影响因子：
4.4
通讯作者：
J. Swarthout;E. Fuhrmeister;Latifah Hamzah;Angela R. Harris;M. A. Ahmed;E. Gurley;S. Satter;A. Boehm;A. Pickering
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文献类型：
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作者：
J. Swarthout;E. Fuhrmeister;Latifah Hamzah;Angela R. Harris;M. A. Ahmed;E. Gurley;S. Satter;A. Boehm;A. Pickering
虽然集约化农业环境和高收入国家已经证明动物肠道微生物群中抗生素耐药性的发展以及随后传播给人类，但缺乏中低收入国家社区中抗生素耐药性人畜共患交换的证据。这项研究提供了人类和动物之间抗生素抗性基因重叠的基因组证据，特别是在城市社区，并强调鸡是抗生素抗性的重要储存库。摘要 低收入和中等收入国家 (LMIC) 承受着最大的抗生素耐药性感染死亡率负担。小规模动物生产和自由放养的家畜在许多中低收入国家很常见，但低收入社区肠道细菌和抗生素抗性基因 (ARG) 人畜共患交换的数据却很少。农村和城市社区在人口密度、抗生素使用和与动物共居方面的差异可能会影响肠道细菌群落和抗逆转录病毒药物在人类和动物之间的传播频率。在这里，我们使用 16S rRNA 基因扩增子测序确定了孟加拉国农村社区与城市社区的人类、鸡和山羊之间肠道微生物组的相似性，并使用长读长宏基因组学确定了抗性组的相似性。与城市社区相比，农村地区（同居现象更常见）的人类和鸡之间的肠道微生物组比城市社区更相似，但农村和城市社区的人类和山羊之间没有差异。城市社区中人类和山羊的抗性基因组更为相似，城市动物中的 ARG 丰度高于农村动物。我们发现，在这两种情况下，人类和动物的 ARG 等位基因存在大量重叠。人类和鸡比人类和山羊有更多的重叠 ARG 等位基因。来自城市社区和农村人群的所有粪便宿主都在染色体重叠群上携带ARG，这些重叠群被归类为潜在致病菌，包括大肠杆菌、空肠弯曲菌、艰难梭菌和肺炎克雷伯菌。这些发现提供了对孟加拉国农村和城市社区人类和动物群体中 ARG 循环广度的深入了解。重要性虽然在集约化农业环境和高收入国家已经证明动物肠道微生物群中抗生素耐药性的发展以及随后传播给人类，但缺乏中低收入国家社区中抗生素耐药性人畜共患交换的证据。这项研究提供了人类和动物之间抗生素抗性基因重叠的基因组证据，特别是在城市社区，并强调鸡是抗生素抗性的重要储存库。在孟加拉国农村地区，鸡和人类的肠道微生物群更加相似，那里的同居现象更为常见。长读长宏基因组学的结合使得能够表征抗性基因的细菌宿主，这在之前仅使用短读长测序的独立于培养物的研究中是不可能的。这些发现强调了制定对抗抗生素耐药性策略的重要性，因为鸡是社区环境中抗抗生素耐药性的储存库，尤其是在城市地区。
While the development of antibiotic resistance in animal gut microbiomes and subsequent transmission to humans has been demonstrated in intensive farming environments and high-income countries, evidence of zoonotic exchange of antibiotic resistance in LMIC communities is lacking. This research provides genomic evidence of overlap of antibiotic resistance genes between humans and animals, especially in urban communities, and highlights chickens as important reservoirs of antibiotic resistance. ABSTRACT Low- and middle-income countries (LMICs) bear the largest mortality burden of antibiotic-resistant infections. Small-scale animal production and free-roaming domestic animals are common in many LMICs, yet data on zoonotic exchange of gut bacteria and antibiotic resistance genes (ARGs) in low-income communities are sparse. Differences between rural and urban communities with regard to population density, antibiotic use, and cohabitation with animals likely influence the frequency of transmission of gut bacterial communities and ARGs between humans and animals. Here, we determined the similarity in gut microbiomes, using 16S rRNA gene amplicon sequencing, and resistomes, using long-read metagenomics, between humans, chickens, and goats in a rural community compared to an urban community in Bangladesh. Gut microbiomes were more similar between humans and chickens in the rural (where cohabitation is more common) than the urban community, but there was no difference for humans and goats in the rural versus the urban community. Human and goat resistomes were more similar in the urban community, and ARG abundance was higher in urban animals than rural animals. We identified substantial overlap of ARG alleles in humans and animals in both settings. Humans and chickens had more overlapping ARG alleles than humans and goats. All fecal hosts from the urban community and rural humans carried ARGs on chromosomal contigs classified as potentially pathogenic bacteria, including Escherichia coli, Campylobacter jejuni, Clostridioides difficile, and Klebsiella pneumoniae. These findings provide insight into the breadth of ARGs circulating within human and animal populations in a rural compared to urban community in Bangladesh. IMPORTANCE While the development of antibiotic resistance in animal gut microbiomes and subsequent transmission to humans has been demonstrated in intensive farming environments and high-income countries, evidence of zoonotic exchange of antibiotic resistance in LMIC communities is lacking. This research provides genomic evidence of overlap of antibiotic resistance genes between humans and animals, especially in urban communities, and highlights chickens as important reservoirs of antibiotic resistance. Chicken and human gut microbiomes were more similar in rural Bangladesh, where cohabitation is more common. Incorporation of long-read metagenomics enabled characterization of bacterial hosts of resistance genes, which has not been possible in previous culture-independent studies using only short-read sequencing. These findings highlight the importance of developing strategies for combatting antibiotic resistance that account for chickens being reservoirs of ARGs in community environments, especially in urban areas.