Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases

Microbiome

Volumn 6, Issue 1, 2018, Pages

  Wu, Zhiqiang ^a,b   Lu, Liang ^c   Du, Jiang ^a   Yang, Li ^a   Ren, Xianwen ^a   Liu, Bo ^a   Jiang, Jinyong ^e   Yang, Jian ^a   Dong, Jie ^a   Sun, Lilian ^a   Zhu, Yafang ^a   Li, Yuhui ^a   Zheng, Dandan ^a   Zhang, Chi ^a   Su, Haoxiang ^a   Zheng, Yuting ^e   Zhou, Hongning ^e   Zhu, Guangjian ^d   Li, Hongying ^d   Chmura, Aleksei ^d   Yang, Fan ^a   Daszak, Peter ^d   Wang, Jianwei ^a,b   Liu, Qiyong ^c   Jin, Qi ^a,b   more..

^a INSTITUTE OF PATHOGEN BIOLOGY   (China)

^b ZHEJIANG UNIVERSITY   (China)

^c CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^d ECOHEALTH ALLIANCE   (United States)

^e Yunnan Institute of Parasitic Diseases   (China)

Author keywords

Emerging infectious diseases; Rodents; Small mammals; Viral evolution; Virome

Indexed keywords

AMINO ACID; DNA POLYMERASE; RNA DIRECTED RNA POLYMERASE; VIRAL PROTEIN;

ADENOVIRIDAE; AMINO ACID SEQUENCE; ANIMAL VIRUS; ARENAVIRIDAE; ARTERIVIRIDAE; ARTICLE; ASTROVIRIDAE; CALICIVIRIDAE; CHINA; CIRCOVIRUS; COMPARATIVE STUDY; CORONAVIRIDAE; DNA VIRUS; FLAVIVIRIDAE; GENE SEQUENCE; GENETIC VARIABILITY; HEPACIVIRUS; HEPATITIS E VIRUS; HERPESVIRIDAE; INSECTIVORA; LAGOMORPH; METAGENOMICS; MOLECULAR EVOLUTION; NEXT GENERATION SEQUENCING; NONHUMAN; PAPILLOMAVIRIDAE; PARAMYXOVIRIDAE; PARVOVIRINAE; PESTIVIRUS; PHYLOGENETIC TREE; PICOBIRNAVIRIDAE; PICORNAVIRIDAE; POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; REVERSE TRANSCRIBING VIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA VIRUS; RODENT; VIRUS GENE; VIRUS GENOME; VIRUS INFECTION; ANIMAL; CLASSIFICATION; COMMUNICABLE DISEASE; GENETICS; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; METAGENOME; VIROLOGY; VIRUS;

ANIMALS; CHINA; COMMUNICABLE DISEASES, EMERGING; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LAGOMORPHA; METAGENOME; RODENTIA; VIRUS DISEASES; VIRUSES;

EID: 85054439206     PISSN: None     EISSN: 20492618     Source Type: Journal    
DOI: 10.1186/s40168-018-0554-9     Document Type: Article

References (71)

1. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases. Nature. 2008;451:990-3.
2. Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Philos Trans R Soc Lond Ser B Biol Sci. 2001;356:983-9.
3. Wu T, Perrings C, Kinzig A, Collins JP, Minteer BA, Daszak P. Economic growth, urbanization, globalization, and the risks of emerging infectious diseases in China: a review. Ambio. 2016;46:18-29.
4. Wolfe ND, Dunavan CP, Diamond J. Origins of major human infectious diseases. Nature. 2007;447:279-83.
5. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JR, Dobson AP, Hudson PJ, Grenfell BT. Epidemic dynamics at the human-animal interface. Science. 2009;326:1362-7.
6. Smith I, Wang LF. Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr Opin Virol. 2013;3:84-91.
7. Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P. Host and viral traits predict zoonotic spillover from mammals. Nature. 2017;546(7660):646-50.
8. Meerburg BG, Singleton GR, Kijlstra A. Rodent-borne diseases and their risks for public health. Crit Rev Microbiol. 2009;35:221-70.
9. Blanga-Kanfi S, Miranda H, Penn O, Pupko T, DeBry RW, Huchon D. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol Biol. 2009;9:71.
10. Wilson DE, Reeder DM. Mammal species of the world: a taxonomic and geographic reference. 3rd ed. Baltimore: Johns Hopkins University Press; 2005.
11. Li K, Lin XD, Wang W, Shi M, Guo WP, Zhang XH, Xing JG, He JR, Wang K, Li MH, et al. Isolation and characterization of a novel arenavirus harbored by rodents and shrews in Zhejiang province, China. Virology. 2015;476:37-42.
12. Guo WP, Lin XD, Wang W, Tian JH, Cong ML, Zhang HL, Wang MR, Zhou RH, Wang JB, Li MH, et al. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog. 2013;9:e1003159.
13. Cao S, Ma J, Cheng C, Ju W, Wang Y. Genetic characterization of hantaviruses isolated from rodents in the port cities of Heilongjiang, China, in 2014. BMC Vet Res. 2016;12:69.
14. Du J, Lu L, Liu F, Su H, Dong J, Sun L, Zhu Y, Ren X, Yang F, Guo F, et al. Distribution and characteristics of rodent picornaviruses in China. Sci Rep. 2016;6:34381.
15. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, Conte JM, Ng J, Garcia J, Bhuva NP, et al. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio. 2014;5:e01933-14.
16. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. The fecal viral flora of wild rodents. PLoS Pathog. 2011;7:e1002218.
17. Feher E, Kemenesi G, Oldal M, Kurucz K, Kugler R, Farkas SL, Marton S, Horvath G, Banyai K, Jakab F. Isolation and complete genome characterization of novel reassortant orthoreovirus from common vole (Microtus arvalis). Virus Genes. 2016;53:307-11.
18. Han BA, Schmidt JP, Bowden SE, Drake JM. Rodent reservoirs of future zoonotic diseases. Proc Natl Acad Sci U S A. 2015;112:7039-44.
19. Palacios G, Druce J, Du L, Tran T, Birch C, Briese T, Conlan S, Quan PL, Hui J, Marshall J, et al. A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med. 2008;358:991-8.
20. Briese T, Paweska JT, McMullan LK, Hutchison SK, Street C, Palacios G, Khristova ML, Weyer J, Swanepoel R, Egholm M, et al. Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog. 2009;5:e1000455.
21. Charrel RN, de Lamballerie X. Zoonotic aspects of arenavirus infections. Vet Microbiol. 2010;140:213-20.
22. Ishii A, Thomas Y, Moonga L, Nakamura I, Ohnuma A, Hang'ombe B, Takada A, Mweene A, Sawa H. Novel arenavirus, Zambia. Emerg Infect Dis. 2011;17:1921-4.
23. Zhang YZ, Zhang FX, Wang JB, Zhao ZW, Li MH, Chen HX, Zou Y, Plyusnin A. Hantaviruses in rodents and humans, Inner Mongolia Autonomous Region, China. Emerg Infect Dis. 2009;15:885-91.
24. Zhang S, Wang S, Yin W, Liang M, Li J, Zhang Q, Feng Z, Li D. Epidemic characteristics of hemorrhagic fever with renal syndrome in China, 2006-2012. BMC Infect Dis. 2014;14:384.
25. Valarcher JF, Hagglund S, Juremalm M, Blomqvist G, Renstrom L, Zohari S, Leijon M, Chirico J. Tick-borne encephalitis. Rev Sci Tech. 2015;34:453-66.
26. Drexler JF, Corman VM, Lukashev AN, van den Brand JM, Gmyl AP, Brunink S, Rasche A, Seggewibeta N, Feng H, Leijten LM, et al. Evolutionary origins of hepatitis A virus in small mammals. Proc Natl Acad Sci U S A. 2015;112:15190-5.
27. Drexler JF, Corman VM, Muller MA, Lukashev AN, Gmyl A, Coutard B, Adam A, Ritz D, Leijten LM, van Riel D, et al. Evidence for novel hepaciviruses in rodents. PLoS Pathog. 2013;9:e1003438.
28. Lau SK, Woo PC, Li KS, Tsang AK, Fan RY, Luk HK, Cai JP, Chan KH, Zheng BJ, Wang M, Yuen KY. Discovery of a novel coronavirus, China Rattus coronavirus HKU24, from Norway rats supports the murine origin of Betacoronavirus 1 and has implications for the ancestor of Betacoronavirus lineage A. J Virol. 2015;89:3076-92.
29. Wang W, Lin XD, Guo WP, Zhou RH, Wang MR, Wang CQ, Ge S, Mei SH, Li MH, Shi M, et al. Discovery, diversity and evolution of novel coronaviruses sampled from rodents in China. Virology. 2015;474:19-27.
30. Wang Y. A complete checklist of mammal species and subspecies in China: a taxonomic and geographic reference. Beijing: China Forestry Publishing House; 2003.
31. Wu Z, Ren X, Yang L, Hu Y, Yang J, He G, Zhang J, Dong J, Sun L, Du J, et al. Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol. 2012;86:10999-1012.
32. Wu Z, Yang L, Ren X, He G, Zhang J, Yang J, Qian Z, Dong J, Sun L, Zhu Y, et al. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J. 2016;10:609-20.
33. Chen L, Liu B, Yang J, Jin Q. DBatVir: the database of bat-associated viruses. Database (Oxford). 2014;2014:bau021.
34. Chen L, Liu B, Wu Z, Jin Q, Yang J. DRodVir: a resource for exploring the virome diversity in rodents. J Genet Genomics. 2017;44:259-64.
35. Woo PC, Lau SK, Wong BH, Wong AY, Poon RW, Yuen KY. Complete genome sequence of a novel paramyxovirus, Tailam virus, discovered in Sikkim rats. J Virol. 2011;85:13473-4.
36. Li Z, Yu M, Zhang H, Magoffin DE, Jack PJ, Hyatt A, Wang HY, Wang LF. Beilong virus, a novel paramyxovirus with the largest genome of non-segmented negative-stranded RNA viruses. Virology. 2006;346:219-28.
37. Jack PJ, Boyle DB, Eaton BT, Wang LF. The complete genome sequence of J virus reveals a unique genome structure in the family Paramyxoviridae. J Virol. 2005;79:10690-700.
38. Klempa B, Kruger DH, Auste B, Stanko M, Krawczyk A, Nickel KF, Uberla K, Stang A. A novel cardiotropic murine adenovirus representing a distinct species of mastadenoviruses. J Virol. 2009;83:5749-59.
39. Hemmi S, Vidovszky MZ, Ruminska J, Ramelli S, Decurtins W, Greber UF, Harrach B. Genomic and phylogenetic analyses of murine adenovirus 2. Virus Res. 2011;160:128-35.
40. Schulz E, Gottschling M, Ulrich RG, Richter D, Stockfleth E, Nindl I. Isolation of three novel rat and mouse papillomaviruses and their genomic characterization. PLoS One. 2012;7:e47164.
41. Schulz E, Gottschling M, Wibbelt G, Stockfleth E, Nindl I. Isolation and genomic characterization of the first Norway rat (Rattus norvegicus) papillomavirus and its phylogenetic position within Pipapillomavirus, primarily infecting rodents. J Gen Virol. 2009;90:2609-14.
42. Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P. Global hotspots and correlates of emerging zoonotic diseases. Nat Commun. 2017;8:1124.
43. Ganesh B, Masachessi G, Mladenova Z. Animal picobirnavirus. Virusdisease. 2014;25:223-38.
44. Manzin A, Mallus F, Macera L, Maggi F, Blois S. Global impact of Torque teno virus infection in wild and domesticated animals. J Infect Dev Ctries. 2015;9:562-70.
45. Manigold T, Vial P. Human hantavirus infections: epidemiology, clinical features, pathogenesis and immunology. Swiss Med Wkly. 2014;144:w13937.
46. Morita C, Tsuchiya K, Ueno H, Muramatsu Y, Kojimahara A, Suzuki H, Miyashita N, Moriwaki K, Jin ML, Wu XL, Wang FS. Seroepidemiological survey of lymphocytic choriomeningitis virus in wild house mice in China with particular reference to their subspecies. Microbiol Immunol. 1996;40:313-5.
47. Blasdell KR, Duong V, Eloit M, Chretien F, Ly S, Hul V, Deubel V, Morand S, Buchy P. Evidence of human infection by a new mammarenavirus endemic to Southeastern Asia. Elife. 2016;5:e13135.
48. Nilubol D, Tripipat T, Hoonsuwan T, Kortheerakul K. Porcine reproductive and respiratory syndrome virus, Thailand, 2010-2011. Emerg Infect Dis. 2012;18:2039-43.
49. An TQ, Tian ZJ, Leng CL, Peng JM, Tong GZ. Highly pathogenic porcine reproductive and respiratory syndrome virus, Asia. Emerg Infect Dis. 2011;17:1782-4.
50. Nelsen CJ, Murtaugh MP, Faaberg KS. Porcine reproductive and respiratory syndrome virus comparison: divergent evolution on two continents. J Virol. 1999;73:270-80.
51. Brar MS, Shi M, Hui RK, Leung FC. Genomic evolution of porcine reproductive and respiratory syndrome virus (PRRSV) isolates revealed by deep sequencing. PLoS One. 2014;9:e88807.
52. Yang L, Wu Z, Ren X, Yang F, He G, Zhang J, Dong J, Sun L, Zhu Y, Du J, et al. Novel SARS-like betacoronaviruses in bats, China, 2011. Emerg Infect Dis. 2013;19:989-91.
53. Yang L, Wu Z, Ren X, Yang F, Zhang J, He G, Dong J, Sun L, Zhu Y, Zhang S, Jin Q. MERS-related betacoronavirus in Vespertilio superans bats, China. Emerg Infect Dis. 2014;20:1260-2.
54. Du J, Yang L, Ren X, Zhang J, Dong J, Sun L, Zhu Y, Yang F, Zhang S, Wu Z, Jin Q. Genetic diversity of coronaviruses in Miniopterus fuliginosus bats. Sci China Life Sci. 2016;59:604-14.
55. Wu Z, Yang L, Ren X, Zhang J, Yang F, Zhang S, Jin Q. ORF8-related genetic evidence for Chinese horseshoe bats as the source of human severe acute respiratory syndrome coronavirus. J Infect Dis. 2016;213:579-83.
56. Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife. 2015;4. https://doi.org/10.7554/eLife.05378.
57. Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, et al. Redefining the invertebrate RNA virosphere. Nature. 2016. https://doi.org/10.1038/nature20167.
58. Carroll D, Daszak P, Wolfe ND, Gao GF, Morel CM, Morzaria S, Pablos-Mendez A, Tomori O, Mazet JAK. The global virome project. Science. 2018;359:872-4.
59. Yang J, Yang F, Ren L, Xiong Z, Wu Z, Dong J, Sun L, Zhang T, Hu Y, Du J, et al. Unbiased parallel detection of viral pathogens in clinical samples by use of a metagenomic approach. J Clin Microbiol. 2011;49:3463-9.
60. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 2011;21:1552-60.
61. Woo PC, Lau SK, Li KS, Poon RW, Wong BH, Tsoi HW, Yip BC, Huang Y, Chan KH, Yuen KY. Molecular diversity of coronaviruses in bats. Virology. 2006;351:180-7.
62. Tang XC, Zhang JX, Zhang SY, Wang P, Fan XH, Li LF, Li G, Dong BQ, Liu W, Cheung CL, et al. Prevalence and genetic diversity of coronaviruses in bats from China. J Virol. 2006;80:7481-90.
63. Chu DK, Poon LL, Guan Y, Peiris JS. Novel astroviruses in insectivorous bats. J Virol. 2008;82:9107-14.
64. Li Y, Ge X, Zhang H, Zhou P, Zhu Y, Zhang Y, Yuan J, Wang LF, Shi Z. Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol. 2010;84:3889-97.
65. Wu Z, Yang L, Yang F, Ren X, Jiang J, Dong J, Sun L, Zhu Y, Zhou H, Jin Q. Novel Henipa-like virus, Mojiang paramyxovirus, in rats, China, 2012. Emerg Infect Dis. 2014;20:1064-6.
66. Zheng XY, Qiu M, Ke XM, Guan WJ, Li JM, Huo ST, Chen SW, Zhong XS, Zhou W, Xiong YQ, et al. Detection of novel adenoviruses in fecal specimens from rodents and shrews in southern China. Virus Genes. 2016;52:417-21.
67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725-9.
68. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A. The delayed rise of present-day mammals. Nature. 2007;446:507-12.
69. Jansa SA, Weksler M. Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phylogenet Evol. 2004;31:256-76.
70. Meredith RW, Janecka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, Goodbla A, Eizirik E, Simao TL, Stadler T, et al. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011;334:521-4.
71. Cui J, Han N, Streicker D, Li G, Tang X, Shi Z, Hu Z, Zhao G, Fontanet A, Guan Y, et al. Evolutionary relationships between bat coronaviruses and their hosts. Emerg Infect Dis. 2007;13:1526-32.