He Tangtian, Xie Jiawen, Jin Ling, Zhao Jue, Zhang Xiaohua, Liu Hang, Li Xiang Dong
Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China.
Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China; Department of Health Technology and Informatics, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China; The Hong Kong Polytechnic University Shenzhen Research Institute, Shenzhen 518057, China.
Environ Int. 2024 Dec;194:109155. doi: 10.1016/j.envint.2024.109155. Epub 2024 Nov 17.
Inhalable microorganisms in airborne fine particulate matter (PM), including bacteria and phages, are major carriers of antibiotic resistance genes (ARGs) with strong ecological linkages and potential health implications for urban populations. A full-spectrum study on ARG carriers and phage-bacterium linkages will shed light on the environmental processes of antibiotic resistance from airborne dissemination to the human lung microbiome. Our metagenomic study reveals the seasonal dynamics of phage communities in PM, their impacts on clinically important ARGs, and potential implications for the human respiratory microbiome in selected cities of China. Gene-sharing network comparisons show that air harbours a distinct phage community connected to human- and water-associated viromes, with 57 % of the predicted hosts being potential bacterial pathogens. The ARGs of common antibiotics, e.g., peptide and tetracycline, dominate both the antibiotic resistome associated with bacteria and phages in PM. Over 60 % of the predicted hosts of vARG-carrying phages are potential bacterial pathogens, and about 67 % of these hosts have not been discovered as direct carriers of the same ARGs. The profiles of ARG-carrying phages are distinct among urban sites, but show a significant enrichment in abundance, diversity, temperate lifestyle, and matches of CRISPR (short for 'clustered regularly interspaced short palindromic repeats') to identified bacterial genomes in winter and spring. Moreover, phages putatively carry 52 % of the total mobile genetic element (MGE)-ARG pairs with a unique 'flu season' pattern in urban areas. This study highlights the role that phages play in the airborne dissemination of ARGs and their delivery of ARGs to specific opportunistic pathogens in human lungs, independent of other pathways of horizontal gene transfer. Natural and anthropogenic stressors, particularly wind speed, UV index, and level of ozone, potentially explained over 80 % of the seasonal dynamics of phage-bacterial pathogen linkages on antibiotic resistance. Therefore, understanding the phage-host linkages in airborne PM, the full-spectrum of antibiotic resistomes, and the potential human pathogens involved, will be of benefit to protect human health in urban areas.
空气中细颗粒物（PM）中的可吸入微生物，包括细菌和噬菌体，是抗生素抗性基因（ARG）的主要载体，它们与城市人群有着紧密的生态联系，并对其健康具有潜在影响。对ARG载体和噬菌体 - 细菌联系进行全谱研究，将有助于揭示抗生素抗性从空气传播到人类肺部微生物组的环境过程。我们的宏基因组研究揭示了PM中噬菌体群落的季节动态、它们对临床上重要的ARG的影响，以及对中国部分城市人类呼吸道微生物组的潜在影响。基因共享网络比较表明，空气中存在一个与人类和水相关病毒群落相连的独特噬菌体群落，预测宿主中有57%是潜在的细菌病原体。常见抗生素（如肽类和四环素）的ARG在与PM中的细菌和噬菌体相关的抗生素抗性组中占主导地位。携带vARG的噬菌体的预测宿主中超过60%是潜在的细菌病原体，其中约67%的宿主尚未被发现是相同ARG的直接载体。携带ARG的噬菌体的图谱在城市站点之间有所不同，但在冬季和春季，其丰度、多样性、温和生活方式以及CRISPR（“成簇规律间隔短回文重复序列”的缩写）与已鉴定细菌基因组的匹配度均显著富集。此外，噬菌体在城市地区假定携带了52%的总移动遗传元件（MGE）-ARG对，呈现出独特的“流感季节”模式。这项研究突出了噬菌体在ARG空气传播以及将ARG传递到人类肺部特定机会性病原体中的作用，这一作用独立于其他水平基因转移途径。自然和人为应激源，特别是风速、紫外线指数和臭氧水平，可能解释了超过80%的噬菌体 - 细菌病原体对抗生素抗性联系的季节动态。因此，了解空气中PM中的噬菌体 - 宿主联系、抗生素抗性组的全谱以及所涉及的潜在人类病原体，将有助于保护城市地区的人类健康。
