Rattus norvegicus Characterization of Novel Viruses Carried by Commensal Detection of Zoonotic Pathogens and 2014

Norway rats (Rattus norvegicus) are globally distributed and concentrate in urban environments, where they live and feed in closer proximity to human populations than most other mammals. Despite the potential role of rats as reservoirs of zoonotic diseases, the microbial diversity present in urban rat populations remains unexplored. In this study, we used targeted molecular assays to detect known bacterial, viral, and protozoan human pathogens and unbiased high-throughput sequencing to identify novel viruses related to agents of human disease in commensal Norway rats in New York City. We found that these rats are infected with bacterial pathogens known to cause acute or mild gastroenteritis in people, including atypical enteropathogenic Escherichia coli, Clostridium difficile, and Salmonella enterica, as well as infectious agents that have been associated with undifferentiated febrile illnesses, including Bartonella spp., Streptobacillus moniliformis, Leptospira interrogans, and Seoul hantavirus. We also identified a wide range of known and novel viruses from groups that contain important human pathogens, including sapoviruses, cardioviruses, kobuviruses, parechoviruses, rotaviruses, and hepaciviruses. The two novel hepaciviruses discovered in this study replicate in the liver of Norway rats and may have utility in establishing a small animal model of human hepatitis C virus infection. The results of this study demonstrate the diversity of microbes carried by commensal rodent species and highlight the need for improved pathogen surveillance and disease monitoring in urban environments. IMPORTANCE The observation that most emerging infectious diseases of humans originate in animal reservoirs has led to widescale microbial surveillance and discovery programs in wildlife, particularly in the developing world. Strikingly, less attention has been focused on commensal animals like rats, despite their abundance in urban centers and close proximity to human populations. To begin to explore the zoonotic disease risk posed by urban rat populations, we trapped and surveyed Norway rats collected in New York City over a 1-year period. This analysis revealed a striking diversity of known pathogens and novel viruses in our study population, including multiple agents associated with acute gastroenteritis or febrile illnesses in people. Our findings indicate that urban rats are reservoirs for a vast diversity of microbes that may affect human health and indicate a need for increased surveillance and awareness of the disease risks associated with urban rodent infestation. Received 11 September 2014 Accepted 15 September 2014 Published 14 October 2014 Citation Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, Conte JM, Ng J, Garcia J, Bhuva NP, Lee B, Che X, Quan P-L, Lipkin WI. 2014. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. mBio 5(5):e01933-14. doi:10.1128/mBio.01933-14. Editor Anne Moscona, Weill Cornell Medical College Copyright © 2014 Firth et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. Address correspondence to Cadhla Firth, cadhla.firth@csiro.au. Zoonotic pathogens comprise a significant and increasing proportion of all new and emerging human infectious diseases (1, 2). Although zoonotic transmission is influenced by many factors, the frequency of contact between animal reservoirs and the human population appears to be a key element (3). Therefore, the risk of zoonotic transmission is increased by events that act to reduce the geographic or ecological separation between human and animal populations or increase the density and abundance of these populations where they coexist (2, 4). In this context, rapid and continuous urbanization constitutes a significant challenge to human health, as it creates irreversible changes to biodiversity that are driven by varied responses from animal species. In particular, species classified as urban exploiters and urban adapters may exist in unnaturally large and dense populations within urban environments and have above-average rates of contact with people (5–7). Of these, few species have been as successful at adapting to a peridomestic lifestyle as the Norway rat (Rattus norvegicus). In the urban environment, Norway rats closely cohabitate with humans—living inside buildings, feeding on refuse, and coming into contact with many aspects of the food supply (7–9). These characteristics, coupled with high levels of fecundity, growth rates, and population densities, suggest that urban Norway rats may be an important source of zoonotic pathogens (10, 11). Indeed, the Norway rat is a known reservoir of a range of human pathogens, including hantaviruses, Bartonella spp., and Leptospira interrogans; however, little is known about the microbial diversity presRESEARCH ARTICLE crossmark September/October 2014 Volume 5 Issue 5 e01933-14 ® mbio.asm.org 1 m b.asm .rg on O cber 4, 2014 P ubished by m b.asm .rg D ow nladed fom