The Influence of Habitat on Viral Diversity in Neotropical Rodent Hosts.

Sourakhata Tirera, Benoit de Thoisy, Damien Donato, Christiane Bouchier, Vincent Lacoste, Alain Franc, Anne Lavergne
Author Information
  1. Sourakhata Tirera: Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, BP 6010, 97306 Cayenne, France. ORCID
  2. Benoit de Thoisy: Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, BP 6010, 97306 Cayenne, France. ORCID
  3. Damien Donato: Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, BP 6010, 97306 Cayenne, France.
  4. Christiane Bouchier: Institut Pasteur, 25-28 Rue du Docteur Roux, CEDEX 15, 75724 Paris, France.
  5. Vincent Lacoste: Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, BP 6010, 97306 Cayenne, France. ORCID
  6. Alain Franc: UMR BIOGECO, INRAE, University Bordeaux, 33612 Cestas, France.
  7. Anne Lavergne: Laboratoire des Interactions Virus-Hôtes, Institut Pasteur de la Guyane, BP 6010, 97306 Cayenne, France.

Abstract

Rodents are important reservoirs of numerous viruses, some of which have significant impacts on public health. Ecosystem disturbances and decreased host species richness have been associated with the emergence of zoonotic diseases. In this study, we aimed at (a) characterizing the viral diversity in seven neotropical rodent species living in four types of habitats and (b) exploring how the extent of environmental disturbance influences this diversity. Through a metagenomic approach, we identified 77,767 viral sequences from spleen, kidney, and serum samples. These viral sequences were attributed to 27 viral families known to infect vertebrates, invertebrates, plants, and amoeba. Viral diversities were greater in pristine habitats compared with disturbed ones, and lowest in peri-urban areas. High viral richness was observed in savannah areas. Differences in these diversities were explained by rare viruses that were generally more frequent in pristine forest and savannah habitats. Moreover, changes in the ecology and behavior of rodent hosts, in a given habitat, such as modifications to the diet in disturbed vs. pristine forests, are major determinants of viral composition. Lastly, the phylogenetic relationships of four vertebrate-related viral families (, , , and ) highlighted the wide diversity of these viral families, and in some cases, a potential risk of transmission to humans. All these findings provide significant insights into the diversity of rodent viruses in Amazonia, and emphasize that habitats and the host's dietary ecology may drive viral diversity. Linking viral richness and abundance to the ecology of their hosts and their responses to habitat disturbance could be the starting point for a better understanding of viral emergence and for future management of ecosystems.

Keywords

References

  1. Mol Biol Evol. 2018 Jun 1;35(6):1547-1549 [PMID: 29722887]
  2. Arch Med Res. 2002 Jul-Aug;33(4):330-42 [PMID: 12234522]
  3. An Acad Bras Cienc. 2020 Apr 17;92(1):e20191375 [PMID: 32321030]
  4. Annu Rev Virol. 2016 Sep 29;3(1):53-75 [PMID: 27741408]
  5. Emerg Microbes Infect. 2014 Mar;3(3):e21 [PMID: 26038514]
  6. Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9423-9430 [PMID: 32284401]
  7. J Mammal. 2016 Jun 9;97(3):663-688 [PMID: 29692469]
  8. Ann N Y Acad Sci. 2017 Feb;1389(1):124-146 [PMID: 28036113]
  9. Nature. 2008 Feb 21;451(7181):990-3 [PMID: 18288193]
  10. J Gen Virol. 2017 Nov;98(11):2771-2785 [PMID: 28984241]
  11. Virus Evol. 2018 Jun 08;4(1):vey016 [PMID: 29942656]
  12. Rev Soc Bras Med Trop. 2020 Feb 07;53:e20190486 [PMID: 32049206]
  13. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5278-81 [PMID: 7777497]
  14. Mol Ecol Resour. 2008 May;8(3):471-9 [PMID: 21585824]
  15. Community Ecol. 2018;19(2):168-175 [PMID: 32218712]
  16. Antiviral Res. 2012 Jun;94(3):242-57 [PMID: 22522323]
  17. Nat Methods. 2012 Jul 30;9(8):772 [PMID: 22847109]
  18. PLoS Pathog. 2013;9(6):e1003438 [PMID: 23818848]
  19. J Infect Dis. 2018 Nov 22;218(suppl_5):S698-S704 [PMID: 30321368]
  20. J Gen Virol. 2017 Jun;98(6):1159-1160 [PMID: 28640744]
  21. Bioinformatics. 2015 May 15;31(10):1674-6 [PMID: 25609793]
  22. Arch Virol. 2018 Oct;163(10):2913-2915 [PMID: 29931397]
  23. mBio. 2018 Apr 17;9(2): [PMID: 29666290]
  24. Emerg Infect Dis. 2005 May;11(5):663-9 [PMID: 15890116]
  25. Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):7039-44 [PMID: 26038558]
  26. J Gen Virol. 2017 Apr;98(4):585-594 [PMID: 28141497]
  27. Nat Biotechnol. 2021 May;39(5):578-585 [PMID: 33349699]
  28. J Hepatol. 2019 Mar;70(3):501-520 [PMID: 30472320]
  29. Virus Evol. 2020 Aug 25;6(2):veaa065 [PMID: 33365150]
  30. Nature. 2018 Apr;556(7700):197-202 [PMID: 29618816]
  31. Emerg Infect Dis. 2017 Oct;23(10):1722-1725 [PMID: 28930019]
  32. Arch Virol. 2016 Jun;161(6):1739-50 [PMID: 26923930]
  33. mBio. 2013 Apr 09;4(2):e00216-13 [PMID: 23572554]
  34. Emerg Infect Dis. 2004 Dec;10(12):2067-72 [PMID: 15663840]
  35. Annu Rev Entomol. 2004;49:141-74 [PMID: 14651460]
  36. Emerg Infect Dis. 2010 Apr;16(4):739-41 [PMID: 20350412]
  37. Sci Total Environ. 2021 Aug 20;783:147090 [PMID: 33872911]
  38. Vaccine. 2005 Feb 18;23(13):1615-23 [PMID: 15694514]
  39. Clin Infect Dis. 2000 Jan;30(1):188-90 [PMID: 10619752]
  40. Nature. 2003 Apr 17;422(6933):714-6 [PMID: 12700760]
  41. Nat Rev Microbiol. 2017 Mar;15(3):183-192 [PMID: 28090077]
  42. Arch Virol. 2019 Jul;164(7):1949-1965 [PMID: 31065850]
  43. Infect Genet Evol. 2016 Jan;37:225-30 [PMID: 26631809]
  44. Infect Genet Evol. 2017 Oct;54:18-38 [PMID: 28634106]
  45. Virologie (Montrouge). 2017 Jun 1;21(3):E12-E27 [PMID: 31967562]
  46. Crit Rev Microbiol. 2009;35(3):221-70 [PMID: 19548807]
  47. Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11609-14 [PMID: 11562506]
  48. Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):12115-20 [PMID: 16880384]
  49. J Virol. 2020 Apr 16;94(9): [PMID: 32075934]
  50. Sci Rep. 2015 Oct 07;5:14830 [PMID: 26445169]
  51. Microbiome. 2018 Oct 3;6(1):178 [PMID: 30285857]
  52. Viruses. 2019 Oct 10;11(10): [PMID: 31658738]
  53. Methods. 2016 Jun 1;102:3-11 [PMID: 27012178]
  54. J Virol. 2012 May;86(9):5399 [PMID: 22492924]
  55. Arch Virol. 2018 Nov;163(11):3203-3206 [PMID: 30097743]
  56. PLoS Pathog. 2016 Apr 19;12(4):e1005574 [PMID: 27093155]
  57. Science. 2018 Feb 23;359(6378):872-874 [PMID: 29472471]
  58. Arch Virol. 2019 Sep;164(9):2401-2410 [PMID: 31243554]
  59. J Genet Genomics. 2017 May 20;44(5):259-264 [PMID: 28533016]
  60. Microbiome. 2021 Jan 21;9(1):18 [PMID: 33478588]
  61. Ecohealth. 2015 Jun;12(2):339-46 [PMID: 25217336]
  62. Virus Res. 2012 Feb;163(2):439-47 [PMID: 22108583]
  63. Viruses. 2020 Apr 09;12(4): [PMID: 32283670]
  64. Science. 1974 Jul 19;185(4147):263-5 [PMID: 4833828]
  65. PLoS One. 2009;4(5):e5461 [PMID: 19421313]
  66. Emerg Infect Dis. 2004 May;10(5):880-8 [PMID: 15200823]
  67. Syst Biol. 2012 May;61(3):539-42 [PMID: 22357727]
  68. Nature. 2016 Sep 29;537(7622):689-693 [PMID: 27654921]
  69. mBio. 2014 Oct 14;5(5):e01933-14 [PMID: 25316698]
  70. Emerg Infect Dis. 2017 May;23(5):872-874 [PMID: 28418305]
  71. Mol Ecol. 2020 Jan;29(1):26-39 [PMID: 31561274]
  72. Am J Trop Med Hyg. 2014 Jun;90(6):988-92 [PMID: 24752689]
  73. Bioinformatics. 2003 Aug 12;19(12):1572-4 [PMID: 12912839]
  74. Bioinformatics. 2011 Apr 15;27(8):1164-5 [PMID: 21335321]
  75. J Vector Ecol. 2004 Jun;29(1):177-91 [PMID: 15266755]
  76. Vet Microbiol. 2013 Nov 29;167(1-2):145-50 [PMID: 23968890]
  77. Annu Rev Virol. 2016 Sep 29;3(1):197-214 [PMID: 27741409]
  78. J Gen Virol. 2015 Aug;96(8):2079-2085 [PMID: 25934793]
  79. Antiviral Res. 2015 Mar;115:83-93 [PMID: 25545071]
  80. J Gen Virol. 2019 Jun;100(6):938-949 [PMID: 31050631]
  81. Am J Trop Med Hyg. 2020 Jan;102(1):195-201 [PMID: 31769401]
  82. Zoonoses Public Health. 2018 Nov;65(7):755-765 [PMID: 30105852]
  83. J Infect Dis. 1997 Apr;175(4):828-32 [PMID: 9086137]
  84. Emerg Infect Dis. 2009 Apr;15(4):519-25 [PMID: 19331726]
  85. Viruses. 2019 Mar 24;11(3): [PMID: 30909631]
  86. Proc Natl Acad Sci U S A. 1988 Jan;85(1):156-9 [PMID: 16578826]
  87. Parasit Vectors. 2018 Jul 11;11(1):405 [PMID: 29996902]
  88. J Gen Virol. 2014 Dec;95(Pt 12):2734-2747 [PMID: 25121550]
  89. Mol Phylogenet Evol. 2001 Aug;20(2):238-51 [PMID: 11476632]
  90. Future Virol. 2011;6(6):721-740 [PMID: 21765860]
  91. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  92. J Virol. 2010 Oct;84(19):9733-48 [PMID: 20660197]
  93. PLoS Pathog. 2011 Sep;7(9):e1002218 [PMID: 21909269]
  94. Nature. 2016 Dec 22;540(7634):539-543 [PMID: 27880757]
  95. Rev Sci Tech. 2017 Aug;36(2):435-444 [PMID: 30152473]
  96. PLoS Med. 2012;9(12):e1001354 [PMID: 23239944]
  97. Oecologia. 2018 Sep;188(1):289-302 [PMID: 29936542]
  98. BMC Bioinformatics. 2014 Nov 19;15:366 [PMID: 25408143]
  99. Nature. 2013 Jun 20;498(7454):310-1 [PMID: 23783626]
  100. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  101. J Mol Biol. 1990 Oct 5;215(3):403-10 [PMID: 2231712]
  102. Nat Commun. 2017 Oct 24;8(1):1124 [PMID: 29066781]
  103. J Gen Virol. 2016 Nov;97(11):2894-2907 [PMID: 27692039]
  104. Am J Trop Med Hyg. 1980 Sep;29(5):969-83 [PMID: 7435797]
  105. Trends Parasitol. 2016 Jul;32(7):565-577 [PMID: 27316904]
  106. PLoS One. 2017 Nov 8;12(11):e0186943 [PMID: 29117243]

MeSH Term

Animals
Ecology
Ecosystem
Forests
Genetic Variation
Metagenome
Phylogeny
Rodentia
Viruses
Zoonoses

Word Cloud

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