Citation: Youyou Li, Chuanning Tang, Yun Zhang, Zihan Li, Gaoyu Wang, Ruoyan Peng, Yi Huang, Xiaoyuan Hu, Henan Xin, Boxuan Feng, Xuefang Cao, Yongpeng He, Tonglei Guo, Yijun He, Haoxiang Su, Xiuji Cui, Lina Niu, Zhiqiang Wu, Jian Yang, Fan Yang, Gang Lu, Lei Gao, Qi Jin, Meifang Xiao, Feifei Yin, Jiang Du. Diversity and independent evolutionary profiling of rodent-borne viruses in Hainan, a tropical island of China .VIROLOGICA SINICA, 2023, 38(5) : 651-662.  http://dx.doi.org/10.1016/j.virs.2023.08.003

Diversity and independent evolutionary profiling of rodent-borne viruses in Hainan, a tropical island of China

  • The risk of emerging infectious diseases (EID) is increasing globally. More than 60% of EIDs worldwide are caused by animal-borne pathogens. This study aimed to characterize the virome, analyze the phylogenetic evolution, and determine the diversity of rodent-borne viruses in Hainan Province, China. We collected 682 anal and throat samples from rodents, combined them into 28 pools according to their species and location, and processed them for next-generation sequencing and bioinformatics analysis. The diverse viral contigs closely related to mammals were assigned to 22 viral families. Molecular clues of the important rodent-borne viruses were further identified by polymerase chain reaction for phylogenetic analysis and annotation of genetic characteristics such as arenavirus, coronavirus, astrovirus, pestivirus, parvovirus, and papillomavirus. We identified pestivirus and bocavirus in Leopoldoms edwardsi from Huangjinjiaoling, and bocavirus in Rattus andamanensis from the national nature reserves of Bangxi with low amino acid identity to known pathogens are proposed as the novel species, and their rodent hosts have not been previously reported to carry these viruses. These results expand our knowledge of viral classification and host range and suggest that there are highly diverse, undiscovered viruses that have evolved independently in their unique wildlife hosts in inaccessible areas.

  • 加载中
  • 10.1016j.virs.2023.08.003-ESM1.xlsx
    10.1016j.virs.2023.08.003-ESM2.xlsx
    10.1016j.virs.2023.08.003-ESM10.xlsx
    10.1016j.virs.2023.08.003-ESM9.xlsx
    10.1016j.virs.2023.08.003-ESM8.xlsx
    10.1016j.virs.2023.08.003-ESM4.xlsx
    10.1016j.virs.2023.08.003-ESM6.xlsx
    10.1016j.virs.2023.08.003-ESM12.docx
    10.1016j.virs.2023.08.003-ESM3.xlsx
    10.1016j.virs.2023.08.003-ESM11.xlsx
    10.1016j.virs.2023.08.003-ESM5.xlsx
    10.1016j.virs.2023.08.003-ESM7.xlsx
    1. Ahmels M, Mariz FC, Braspenning-Wesch I, Stephan S, Huber B, Schmidt G, Cao R, Müller M, Kirnbauer R, Rösl F, Hasche D. 2022. Next generation l2-based hpv vaccines cross-protect against cutaneous papillomavirus infection and tumor development. Front Immunol, 13:1010790.

    2. Allander T, Tammi M, Eriksson M, Bjerkner A, Tiveljung-Lindell A, Andersson B. 2005. Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proceedings of the National Academy of Sciences, 102:12891-12896.

    3. Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P. 2017. Global hotspots and correlates of emerging zoonotic diseases. Nat Commun, 8:1124.

    4. Blasdell KR, Wynne JW, Perera D, Firth C. 2021. First detection of a novel 'unknown host' flavivirus in a malaysian rodent. Access Microbiol, 3:000223.

    5. Blinkova O, Kapoor A, Victoria J, Jones M, Wolfe N, Naeem A, Shaukat S, Sharif S, Alam MM, Angez M, Zaidi S, Delwart EL. 2009. Cardioviruses are genetically diverse and cause common enteric infections in south asian children. J Virol, 83:4631-4641.

    6. Calderón A, Guzmán C, Oviedo-Socarras T, Mattar S, Rodríguez V, Castañeda V, Moraes Figueiredo LT. 2021. Two cases of natural infection of dengue-2 virus in bats in the colombian caribbean. Trop Med Infect Dis, 6:35.

    7. Calistri A, Palù G. 2015. Editorial commentary:Unbiased next-generation sequencing and new pathogen discovery:Undeniable advantages and still-existing drawbacks. Clin Infect Dis, 60:889-891.

    8. Calvignac-Spencer S, Kouadio L, Couacy-Hymann E, Sogoba N, Rosenke K, Davison AJ, Leendertz F, Jarvis MA, Feldmann H, Ehlers B. 2020. Multiple DNA viruses identified in multimammate mouse (mastomys natalensis) populations from across regions of sub-saharan africa. Arch Virol, 165:2291-2299.

    9. Cheever FS, Daniels JB, et al. 1949. A murine virus (jhm) causing disseminated encephalomyelitis with extensive destruction of myelin. J Exp Med, 90:181-210.

    10. Dema A, Tallapally MR, Ganji VK, Buddala B, Kodi H, Ramidi A, Yella NR, Putty K. 2023. A comprehensive molecular survey of viral pathogens associated with canine gastroenteritis. Arch Virol, 168:36.

    11. Eaton K, Featherstone L, Duchene S, Carmichael AG, Varlık N, Golding GB, Holmes EC, Poinar HN. 2023. Plagued by a cryptic clock:Insight and issues from the global phylogeny of yersinia pestis. Commun Biol, 6:23.

    12. Fang LZ, Xiao X, Lei SC, Liu JW, Yu XJ. 2023. Haemaphysalis flava ticks as a competent vector of severe fever with thrombocytopenia syndrome virus. Ticks Tick Borne Dis, 14:102100.

    13. 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 PL, Lipkin WI. 2014. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal rattus norvegicus in new york city. mBio, 5:e01933-01914.

    14. Geldenhuys M, Weyer J, Kearney T, Markotter W. 2022. Host-associated distribution of two novel mammarenaviruses in rodents from southern africa. Viruses, 15:99.

    15. Guo WP, Lin XD, Wang W, Tian JH, Cong ML, Zhang HL, Wang MR, Zhou RH, Wang JB, Li MH, Xu J, Holmes EC, Zhang YZ. 2013. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog, 9:e1003159.

    16. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A. 2013. De novo transcript sequence reconstruction from rna-seq using the trinity platform for reference generation and analysis. Nat Protoc, 8:1494-1512.

    17. Haro-Moreno JM, Cabello-Yeves PJ, Garcillán-Barcia MP, Zakharenko A, Zemskaya TI, Rodriguez-Valera F. 2023. A novel and diverse group of candidatus patescibacteria from bathypelagic lake baikal revealed through long-read metagenomics. Environ Microbiome, 18:12.

    18. Ho HT, Peischard S, Strutz-Seebohm N, Seebohm G. 2021. Virus-host interactions of enteroviruses and parvovirus b19 in myocarditis. Cell Physiol Biochem, 55:679-703.

    19. Huang C, Kolokoltsova OA, Mateer EJ, Koma T, Paessler S. 2017. Highly pathogenic new world arenavirus infection activates the pattern recognition receptor protein kinase r without attenuating virus replication in human cells. J Virol, 91:e01090-17.

    20. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature, 451:990-993.

    21. Kavela S, Vyas P, Cp J, Kushwaha SK, Majumdar SS, Faisal SM. 2023. Use of an integrated multi-omics approach to identify molecular mechanisms and critical factors involved in the pathogenesis of leptospira. Microbiol Spectr:e0313522.

    22. Li H, Durbin R. 2010. Fast and accurate long-read alignment with burrows-wheeler transform. Bioinformatics, 26:589-595.

    23. Li X, Wang L, Liu P, Li H, Huo S, Zong K, Zhu S, Guo Y, Zhang L, Hu B, Lan Y, Chmura A, Wu G, Daszak P, Liu WJ, Gao GF. 2021. A novel potentially recombinant rodent coronavirus with a polybasic cleavage site in the spike protein. J Virol, 95:e0117321.

    24. Liu Q, He B, Huang S-Y, Wei F, Zhu X-Q. 2014. Severe fever with thrombocytopenia syndrome, an emerging tick-borne zoonosis. The Lancet Infectious Diseases, 14:763-772.

    25. Liu S, Zhang T. 2023. A long-term retrospective analysis of the haemorrhagic fever with renal syndrome epidemic from 2005 to 2021 in jiangxi province, china. Sci Rep, 13:2268.

    26. Mietzsch M, Penzes JJ, Agbandje-McKenna M. 2019. Twenty-five years of structural parvovirology. Viruses, 11:362.

    27. Parker JC, Cross SS, Rowe WP. 1970. Rat coronavirus (rcv):A prevalent, naturally occurring pneumotropic virus of rats. Arch Gesamte Virusforsch, 31:293-302.

    28. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL. 2011. The fecal viral flora of wild rodents. PLoS Pathog, 7:e1002218.

    29. Piche-Ovares M, Romero-Vega M, Vargas-González D, Murillo DFB, Soto-Garita C, Francisco-Llamas J, Alfaro-Alarcón A, Jiménez C, Corrales-Aguilar E. 2022. Serosurvey in two dengue hyperendemic areas of costa rica evidence active circulation of wnv and slev in peri-domestic and domestic animals and in humans. Pathogens, 12:7.

    30. Pulkkinen LIA, Butcher SJ, Anastasina M. 2018. Tick-borne encephalitis virus:A structural view. Viruses, 10:350.

    31. Ren LL, Wang YM, Wu ZQ, Xiang ZC, Guo L, Xu T, Jiang YZ, Xiong Y, Li YJ, Li XW, Li H, Fan GH, Gu XY, Xiao Y, Gao H, Xu JY, Yang F, Wang XM, Wu C, Chen L, Liu YW, Liu B, Yang J, Wang XR, Dong J, Li L, Huang CL, Zhao JP, Hu Y, Cheng ZS, Liu LL, Qian ZH, Qin C, Jin Q, Cao B, Wang JW. 2020. Identification of a novel coronavirus causing severe pneumonia in human:A descriptive study. Chin Med J (Engl), 133:1015-1024.

    32. Saito T, Hattori T, Okuya K, Manzoor R, Miyamoto H, Kajihara M, Takada A. 2021. Molecular mechanisms underlying the cellular entry and host range restriction of lujo virus. mBio, 13:e0306021.

    33. Schirtzinger EE, Suddith AW, Hause BM, Hesse RA. 2015. First identification of porcine parvovirus 6 in north america by viral metagenomic sequencing of serum from pigs infected with porcine reproductive and respiratory syndrome virus. Virol J, 12:170.

    34. Smith DB, Becher P, Bukh J, Gould EA, Meyers G, Monath T, Muerhoff AS, Pletnev A, Rico-Hesse R, Stapleton JT, Simmonds P. 2016. Proposed update to the taxonomy of the genera hepacivirus and pegivirus within the family flaviviridae. Virus taxonomyghth report of the international committee on taxonomy family. J Gen Virol, 97:2894-2907.

    35. Tang K, Zhang Y, Zhang C, Hu H, Zhuang R, Jin B, Zhang Y, Ma Y. 2023. Hantaan virus-induced elevation of plasma osteoprotegerin and its clinical implications in hemorrhagic fever with renal syndrome. Int J Infect Dis, 126:14-21.

    36. Wang G, Huang Y, Zhang W, Peng R, Luo J, Liu S, Bai S, Hu X, Wu Z, Yang F, Shen S, Zhang Y, Tang C, Cui X, Niu L, Lu G, Li S, Deng F, Zhang P, Du J, Yin F. 2021. Identification and genome analysis of a novel picornavirus from captive belugas (delphinapterus leucas) in china. Sci Rep, 11:21018.

    37. Wang X, Ren Z, Wang L, Chen J, Zhang P, Chen JP, Chen X, Li L, Lin X, Qi N, Luo S, Xiang R, Yuan Z, Zhang J, Wang G, Sun MH, Huang Y, Hua Y, Zou J, Hou F, Huang Z, Du S, Xiang H, Sun M, Liu Q, Liao M. 2022. Identification of coronaviruses in farmed wild animals reveals their evolutionary origins in guangdong, southern china. Virus Evol, 8:veac049.

    38. Wood R, Bangura U, Mariën J, Douno M, Fichet-Calvet E. 2021. Detection of lassa virus in wild rodent feces:Implications for lassa fever burden within households in the endemic region of faranah, guinea. One Health, 13:100317.

    39. Wu T, Perrings C, Kinzig A, Collins JP, Minteer BA, Daszak P. 2017. Economic growth, urbanization, globalization, and the risks of emerging infectious diseases in china:A review. Ambio, 46:18-29.

    40. Wu Z, Du J, Lu L, Yang L, Dong J, Sun L, Zhu Y, Liu Q, Jin Q. 2018a. Detection of hantaviruses and arenaviruzses in three-toed jerboas from the inner mongolia autonomous region, china. Emerg Microbes Infect, 7:35.

    41. Wu Z, Liu B, Du J, Zhang J, Lu L, Zhu G, Han Y, Su H, Yang L, Zhang S, Liu Q, Jin Q. 2018b. Discovery of diverse rodent and bat pestiviruses with distinct genomic and phylogenetic characteristics in several chinese provinces. Front Microbiol, 9:2562.

    42. Wu Z, Ren X, Yang L, Hu Y, Yang J, He G, Zhang J, Dong J, Sun L, Du J, Liu L, Xue Y, Wang J, Yang F, Zhang S, Jin Q. 2012. Virome analysis for identification of novel mammalian viruses in bat species from chinese provinces. J Virol, 86:10999-11012.

    43. Wu Z, Lu L, Du J, Yang L, Ren X, Liu B, Jiang J, Yang J, Dong J, Sun L, Zhu Y, Li Y, Zheng D, Zhang C, Su H, Zheng Y, Zhou H, Zhu G, Li H, Chmura A, Yang F, Daszak P, Wang J, Liu Q, Jin Q. 2018c. Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases. Microbiome, 6:178.

    44. Wu Z, Han Y, Liu B, Li H, Zhu G, Latinne A, Dong J, Sun L, Su H, Liu L, Du J, Zhou S, Chen M, Kritiyakan A, Jittapalapong S, Chaisiri K, Buchy P, Duong V, Yang J, Jiang J, Xu X, Zhou H, Yang F, Irwin DM, Morand S, Daszak P, Wang J, Jin Q. 2021. Decoding the rna viromes in rodent lungs provides new insight into the origin and evolutionary patterns of rodent-borne pathogens in mainland southeast asia. Microbiome, 9:18.

    45. Xu LD, Zhang F, Chen C, Peng L, Luo WT, Chen R, Xu P, Huang YW. 2022. Revisiting the mongolian gerbil model for hepatitis e virus by reverse genetics. Microbiol Spectr, 10:e0219321.

    46. Zell R, Delwart E, Gorbalenya AE, Hovi T, King AMQ, Knowles NJ, Lindberg AM, Pallansch MA, Palmenberg AC, Reuter G, Simmonds P, Skern T, Stanway G, Yamashita T, Ictv Report C. 2017. Ictv virus taxonomy profile:Picornaviridae. J Gen Virol, 98:2421-2422.

    47. Zhang Y, Rao L, Lv G, Zhang L, Fu R, Wang S, Wu Y, Cui X, Yin F. 2018. Complete genome sequence of a mammarenavirus harbored by rodents on hainan island, china. Genome Announc, 6:e00129-18.

    48. Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL. 2020. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, 579:270-273.

    49. Zhu W, Yang J, Lu S, Jin D, Wu S, Pu J, Luo XL, Liu L, Li Z, Xu J. 2021. Discovery and evolution of a divergent coronavirus in the plateau pika from china that extends the host range of alphacoronaviruses. Front Microbiol, 12:755599.

    50. Zhu X, Liu Y, Guo J, Cao J, Wang Z, Xiao G, Wang W. Effects of N-Linked Glycan on Lassa Virus Envelope Glycoprotein Cleavage, Infectivity, and Immune Response. Virol Sin. 36:774-783.

  • 加载中

Article Metrics

Article views(2408) PDF downloads(51) Cited by()

Related
Proportional views

    Diversity and independent evolutionary profiling of rodent-borne viruses in Hainan, a tropical island of China

      Corresponding author: Meifang Xiao, xiaomeifang2006@hotmail.com
      Corresponding author: Feifei Yin, yinfeifeiff@163.com
      Corresponding author: Jiang Du, dujiangemail@163.com
    • a. NHC Key Laboratory of Systems Biology of Pathogens, Institute of Pathogen Biology, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, 100005, China;
    • b. Department of Clinical Laboratory, Center for Laboratory Medicine, Hainan Women and Children's Medical Center, Haikou, 571199, China;
    • c. Key Laboratory of Tropical Translational Medicine of Ministry of Education, Hainan Medical University, Haikou, 571199, China;
    • d. Hainan Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, Haikou, 571199, China;
    • e. Department of Pathogen Biology, Hainan Medical University, Haikou, 571199, China

    Abstract: The risk of emerging infectious diseases (EID) is increasing globally. More than 60% of EIDs worldwide are caused by animal-borne pathogens. This study aimed to characterize the virome, analyze the phylogenetic evolution, and determine the diversity of rodent-borne viruses in Hainan Province, China. We collected 682 anal and throat samples from rodents, combined them into 28 pools according to their species and location, and processed them for next-generation sequencing and bioinformatics analysis. The diverse viral contigs closely related to mammals were assigned to 22 viral families. Molecular clues of the important rodent-borne viruses were further identified by polymerase chain reaction for phylogenetic analysis and annotation of genetic characteristics such as arenavirus, coronavirus, astrovirus, pestivirus, parvovirus, and papillomavirus. We identified pestivirus and bocavirus in Leopoldoms edwardsi from Huangjinjiaoling, and bocavirus in Rattus andamanensis from the national nature reserves of Bangxi with low amino acid identity to known pathogens are proposed as the novel species, and their rodent hosts have not been previously reported to carry these viruses. These results expand our knowledge of viral classification and host range and suggest that there are highly diverse, undiscovered viruses that have evolved independently in their unique wildlife hosts in inaccessible areas.

    Reference (50) Relative (20)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return