Lei Huaxin, Du Shicong, Tong Xinzhao, Chan Wing Lam, Leung Marcus H Y, Bøifot Kari O, Bezdan Daniela, Butler Daniel J, Danko David C, Green David C, Hernandez Mark T, Kelly Frank J, Lucaci Alexander G, Meydan Cem, Nieto-Caballero Marina, Ryon Krista, Tierney Braden, Udekwu Klas I, Young Benjamin G, Mason Christopher E, Dybwad Marius, Lee Patrick K H
School of Energy and Environment, City University of Hong Kong, Kowloon, Hong Kong SAR, China.
Department of Biological Sciences, School of Sciences, Xi'an Jiaotong-Liverpool University, Suzhou, P.R. China.
Microbiome. 2025 Aug 29;13(1):193. doi: 10.1186/s40168-025-02173-z.
BACKGROUND: There is a diverse assemblage of microbes in air in built environments (BEs), but our understanding of viruses and their interactions with hosts in BEs remains incomplete. To address this knowledge gap, this study analyzed 503 metagenomes isolated from air samples from public transit systems in six global cities, namely Denver, Hong Kong, London, New York City, Oslo, and Stockholm. Viral genomes were recovered from samples via metagenomic binning, and viruses' taxonomy, functional potential, and microbial hosts were determined. The study also investigated correlations between virus and host abundances, the coevolution of clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated (Cas) systems and anti-CRISPR (Acr) proteins, and the potential impacts of auxiliary metabolic genes (AMGs) on hosts. RESULTS: Airborne viruses in global BEs exhibited biogeographical variations in diversity, composition, function, and virus-host interactions. Nearly half of the vOTUs analyzed were from the Caulimoviridae family, while 31.8% of them could not be taxonomically classified. Diverse functions were identified within the vOTUs, together with antimicrobial resistance genes with the potential to confer resistance to various antibiotics and antimicrobial agents. Strong correlations were observed between vOTU and host abundances, with clear distinctions between virulent and temperate viruses. However, there was limited co-evolution of CRISPR-Cas systems and Acr proteins, which was likely due to the oligotrophic and physical conditions in the BEs and the dominance of vOTUs with a virulent lifestyle. Phage-encoded AMGs appeared to have the potential to enhance host fitness. These findings highlight biogeographical variations in airborne viruses in BEs and that physical and oligotrophic conditions in BEs drive virus survival strategies and virus-host coevolution. CONCLUSION: There are biogeographical variations in airborne viruses in BEs in global cities, as physical and oligotrophic conditions in BEs drive virus survival strategies and virus-host coevolution. Moreover, the characteristics of airborne viruses in BEs are distinct from those of viruses found in other, more nutrient-rich ecosystems. Video Abstract.
背景：建筑环境（BEs）中的空气中存在多种多样的微生物群落，但我们对建筑环境中的病毒及其与宿主的相互作用的了解仍不完整。为了填补这一知识空白，本研究分析了从六个全球城市（丹佛、香港、伦敦、纽约市、奥斯陆和斯德哥尔摩）的公共交通系统空气样本中分离出的503个宏基因组。通过宏基因组分箱从样本中回收病毒基因组，并确定病毒的分类学、功能潜力和微生物宿主。该研究还调查了病毒和宿主丰度之间的相关性、成簇规律间隔短回文重复序列（CRISPR）/CRISPR相关（Cas）系统与抗CRISPR（Acr）蛋白的共同进化，以及辅助代谢基因（AMGs）对宿主的潜在影响。 结果：全球建筑环境中的空气传播病毒在多样性、组成、功能和病毒-宿主相互作用方面表现出生物地理变异。分析的近一半病毒操作分类单元（vOTUs）来自花椰菜花叶病毒科，而其中31.8%无法进行分类学分类。在vOTUs中鉴定出了多种功能，以及具有对各种抗生素和抗菌剂产生抗性潜力的抗微生物抗性基因。观察到vOTU与宿主丰度之间存在强相关性，烈性病毒和温和病毒之间有明显区别。然而，CRISPR-Cas系统和Acr蛋白的共同进化有限，这可能是由于建筑环境中的贫营养和物理条件以及具有烈性生活方式的vOTUs占主导地位。噬菌体编码的AMGs似乎有增强宿主适应性的潜力。这些发现突出了建筑环境中空气传播病毒的生物地理变异，以及建筑环境中的物理和贫营养条件驱动病毒生存策略和病毒-宿主共同进化。 结论：全球城市建筑环境中的空气传播病毒存在生物地理变异，因为建筑环境中的物理和贫营养条件驱动病毒生存策略和病毒-宿主共同进化。此外，建筑环境中空气传播病毒的特征与其他营养更丰富的生态系统中发现的病毒特征不同。视频摘要。
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