Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees.
Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys...
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2008
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oai:doaj.org-article:5d62bad5c9814223a588225053c27ca02021-11-25T05:46:31ZMolecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees.1553-73661553-737410.1371/journal.ppat.1000097https://doaj.org/article/5d62bad5c9814223a588225053c27ca02008-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/18604273/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.Weimin LiuMichael WorobeyYingying LiBrandon F KeeleFrederic Bibollet-RucheYuanyuan GuoPaul A GoepfertMario L SantiagoJean-Bosco N NdjangoCecile NeelStephen L CliffordCrickette SanzShadrack KamenyaMichael L WilsonAnne E PuseyNicole Gross-CampChristophe BoeschVince SmithKoichiro ZammaMichael A HuffmanJohn C MitaniDavid P WattsMartine PeetersGeorge M ShawWilliam M SwitzerPaul M SharpBeatrice H HahnPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 4, Iss 7, p e1000097 (2008) |
| institution |
DOAJ |
| collection |
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| language |
EN |
| topic |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
| spellingShingle |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Weimin Liu Michael Worobey Yingying Li Brandon F Keele Frederic Bibollet-Ruche Yuanyuan Guo Paul A Goepfert Mario L Santiago Jean-Bosco N Ndjango Cecile Neel Stephen L Clifford Crickette Sanz Shadrack Kamenya Michael L Wilson Anne E Pusey Nicole Gross-Camp Christophe Boesch Vince Smith Koichiro Zamma Michael A Huffman John C Mitani David P Watts Martine Peeters George M Shaw William M Switzer Paul M Sharp Beatrice H Hahn Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| description |
Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies. |
| format |
article |
| author |
Weimin Liu Michael Worobey Yingying Li Brandon F Keele Frederic Bibollet-Ruche Yuanyuan Guo Paul A Goepfert Mario L Santiago Jean-Bosco N Ndjango Cecile Neel Stephen L Clifford Crickette Sanz Shadrack Kamenya Michael L Wilson Anne E Pusey Nicole Gross-Camp Christophe Boesch Vince Smith Koichiro Zamma Michael A Huffman John C Mitani David P Watts Martine Peeters George M Shaw William M Switzer Paul M Sharp Beatrice H Hahn |
| author_facet |
Weimin Liu Michael Worobey Yingying Li Brandon F Keele Frederic Bibollet-Ruche Yuanyuan Guo Paul A Goepfert Mario L Santiago Jean-Bosco N Ndjango Cecile Neel Stephen L Clifford Crickette Sanz Shadrack Kamenya Michael L Wilson Anne E Pusey Nicole Gross-Camp Christophe Boesch Vince Smith Koichiro Zamma Michael A Huffman John C Mitani David P Watts Martine Peeters George M Shaw William M Switzer Paul M Sharp Beatrice H Hahn |
| author_sort |
Weimin Liu |
| title |
Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| title_short |
Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| title_full |
Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| title_fullStr |
Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| title_full_unstemmed |
Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| title_sort |
molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2008 |
| url |
https://doaj.org/article/5d62bad5c9814223a588225053c27ca0 |
| work_keys_str_mv |
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