Phylogenetic analysis of small ruminant lentiviruses in Germany and Iran suggests their expansion with domestic sheep.

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      Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
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      Original Publication: London : Nature Publishing Group, copyright 2011-
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    • Abstract:
      Small ruminant lentiviruses (SRLVs) are found in sheep in Germany and Iran. SRLVs have been classified into four genotypes: A-C and E. Genotype A has been subdivided into 20 subtypes. Previous studies suggested that, first, the ancestors of genotype A are those SRLVs found in Turkey, second, the evolution of SRLVs is related to the domestication process, and, third, SRLV infection was first observed in sheep in Iceland and the source of that infection was a flock imported from Germany. This study generated, for the first time, partial SRLV sequence data from German and Iranian sheep, enhancing our knowledge of the genetic and evolutionary relationships of SRLVs, and their associations with the domestication process. Based on 54 SRLV sequences from German and Iranian sheep, our results reveal: (1) SRLV subtypes A4, A5, A11, A16 and A21 (new) are found in German sheep and A22 (new) in Iranian sheep. (2) Genotype A has potentially an additional ancestor (A22), found in Iran, Lebanon and Jordan. (3) Subtype A22 is likely an old version of SRLVs. (4) The transmission routes of some SRLVs are compatible with domestication pathways. (5) This study found no evidence of Icelandic subtype A1 in German sheep.
    • References:
      Narayan, O. et al. The lentiviruses of sheep and goats in The Retroviridae 2 (ed. Levy, J.A.) 229–255 (Springer, Boston, MA, 1993). (PMID: 10.1007/978-1-4899-1627-3_4)
      Peterhans, E. et al. Routes of transmission and consequences of small ruminant lentiviruses (SRLVs) infection and eradication schemes. Vet. Res. 35, 257–274, https://doi.org/10.1051/vetres:2004014 (2004). (PMID: 10.1051/vetres:200401415210075)
      Pépin, M., Vitu, C., Russo, P., Mornex, J.-F. & Peterhans, E. Maedi-visna virus infection in sheep: a review. Vet. Res. 29, 341–367, https://hal.archives-ouvertes.fr/hal-00902532 (1998). (PMID: 9689746)
      Shah, C. et al. Phylogenetic analysis and reclassification of caprine and ovine lentiviruses based on 104 new isolates: evidence for regular sheep-to-goat transmission and worldwide propagation through livestock trade. Virology 319, 12–26, https://doi.org/10.1016/j.virol.2003.09.047 (2004). (PMID: 10.1016/j.virol.2003.09.04714967484)
      Reina, R. et al. Prevention strategies against small ruminant lentiviruses: An update. Vet. J. 182, 31–37, https://doi.org/10.1016/j.tvjl.2008.05.008 (2009). (PMID: 10.1016/j.tvjl.2008.05.00818755622)
      Ramírez, H., Reina, R., Amorena, B., de Andrés, D. & Martínez, H. A. Small ruminant Lentiviruses: Genetic variability, tropism and diagnosis. Viruses 5, 1175–1207, https://doi.org/10.3390/v5041175 (2013). (PMID: 10.3390/v5041175236118473705272)
      Minardi da Cruz, J. S., Singh, D., Lamara, A. & Chebloune, Y. Small ruminant lentiviruses (SRLVs) break the species barrier to acquire new host range. Viruses 5, 1867–1884, https://doi.org/10.3390/v5071867 (2013). (PMID: 10.3390/v5071867238812763738966)
      Giammarioli, M. et al. Phylogenetic analysis of small ruminant lentivirus (SRLV) in Italian flocks reveals the existence of novel genetic subtypes. Virus Genes 43, 380–384, https://doi.org/10.1007/s11262-011-0653-1 (2011). (PMID: 10.1007/s11262-011-0653-121858464)
      Grego, E. et al. Genetic characterization of small ruminant lentivirus in Italian mixed flocks: evidence for a novel genotype circulating in a local goat population. J. Gen. Virol. 88, 3423–3427, https://doi.org/10.1099/vir.0.83292-0 (2007). (PMID: 10.1099/vir.0.83292-018024912)
      Kuhar, U., Barlič-Maganja, D. & Grom, J. Phylogenetic analysis of small ruminant lentiviruses detected in Slovenia. Vet. Microbiol. 162, 201–206, https://doi.org/10.1016/j.vetmic.2012.08.024 (2013). (PMID: 10.1016/j.vetmic.2012.08.02423022680)
      Olech, M., Rachid, A., Croisé, B., Kuźmak, J. & Valas, S. Genetic and antigenic characterization of small ruminant lentiviruses circulating in Poland. Virus Res. 163, 528–536, https://doi.org/10.1016/j.virusres.2011.11.019 (2012). (PMID: 10.1016/j.virusres.2011.11.01922155513)
      Olech, M., Valas, S. & Kuźmak, J. Epidemiological survey in single-species flocks from Poland reveals expanded genetic and antigenic diversity of small ruminant lentiviruses. PLoS One 13, e0193892, https://doi.org/10.1371/journal.pone.0193892 (2018). (PMID: 10.1371/journal.pone.0193892295056125837103)
      Olech, M., Murawski, M. & Kuźmak, J. Molecular analysis of small-ruminant lentiviruses in Polish flocks reveals the existence of a novel subtype in sheep. Arch. Virol. 164, 1193–1198, https://doi.org/10.1007/s00705-019-04161-9 (2019). (PMID: 10.1007/s00705-019-04161-9307392016420616)
      Pisoni, G. et al. Genetic analysis of small ruminant lentiviruses following lactogenic transmission. Virology 407, 91–99, https://doi.org/10.1016/j.virol.2010.08.004 (2010). (PMID: 10.1016/j.virol.2010.08.00420797752)
      Colitti, B. et al. A new approach for Small Ruminant Lentivirus full genome characterization revealed the circulation of divergent strains. PLoS One 14, e0212585, https://doi.org/10.1371/journal.pone.0212585 (2019). (PMID: 10.1371/journal.pone.0212585307899506383919)
      Bertolotti, L. et al. Characterization of new small ruminant lentivirus subtype B3 suggests animal trade within the Mediterranean Basin. J. Gen. Virol. 92, 1923–1929, https://doi.org/10.1099/vir.0.032334-0 (2011). (PMID: 10.1099/vir.0.032334-021562119)
      Gjerset, B., Storset, A. K. & Rimstad, E. Genetic diversity of small-ruminant lentiviruses: Characterization of Norwegian isolates of Caprine arthritis encephalitis virus. J. Gen. Virol. 87, 573–580, https://doi.org/10.1099/vir.0.81201-0 (2006). (PMID: 10.1099/vir.0.81201-016476978)
      Gjerset, B., Rimstad, E., Teige, J., Soetaert, K. & Jonassen, C. M. Impact of natural sheep-goat transmission on detection and control of small ruminant lentivirus group C infections. Vet. Microbiol. 135, 231–238, https://doi.org/10.1016/j.vetmic.2008.09.069 (2009). (PMID: 10.1016/j.vetmic.2008.09.06918986775)
      Reina, R. et al. Molecular characterization and phylogenetic study of Maedi Visna and Caprine Arthritis Encephalitis viral sequences in sheep and goats from Spain. Virus Res. 121, 189–198, https://doi.org/10.1016/j.virusres.2006.05.011 (2006). (PMID: 10.1016/j.virusres.2006.05.01116870297)
      Reina, R. et al. Small ruminant lentivirus genotype E is widespread in Sarda goat. Vet. Microbiol. 144, 24–31, https://doi.org/10.1016/j.vetmic.2009.12.020 (2010). (PMID: 10.1016/j.vetmic.2009.12.02020060658)
      Gifford, R. J. Viral evolution in deep time: lentiviruses and mammals. Trends Genet. 28, 89–100, https://doi.org/10.1016/j.tig.2011.11.003 (2012). (PMID: 10.1016/j.tig.2011.11.00322197521)
      Zhang, C., De Silva, S., Wang, J.-H. & Wu, L. Co-evolution of primate SAMHD1 and lentivirus Vpx leads to the loss of the vpx gene in HIV-1 ancestor. PLoS One 7, e37477, https://doi.org/10.1371/journal.pone.0037477 (2012). (PMID: 10.1371/journal.pone.0037477225742283345027)
      Yamada, E. et al. A naturally occurring bovine APOBEC3 confers resistance to bovine lentiviruses: implication for the co-evolution of bovids and their lentiviruses. Sci. Rep. 6, 33988, https://doi.org/10.1038/srep33988 (2016). (PMID: 10.1038/srep33988276657245036201)
      Takeuchi, J. S. et al. Coevolutionary dynamics between tribe Cercopithecini tetherins and their lentiviruses. Sci. Rep. 5, 16021, https://doi.org/10.1038/srep16021 (2015). (PMID: 10.1038/srep16021265317274631996)
      Worobey, M. et al. Island biogeography reveals the deep history of SIV. Science 329, 1487, https://doi.org/10.1126/science.1193550 (2010). (PMID: 10.1126/science.119355020847261)
      Garcia-Etxebarria, K., Sistiaga-Poveda, M. & Marina Jugo, B. Endogenous retroviruses in domestic animals. Curr Genomics 15, 256–265 (2014). (PMID: 10.2174/1389202915666140520003503)
      Chessa, B. et al. Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532–536, https://doi.org/10.1126/science.1170587 (2009). (PMID: 10.1126/science.1170587193900513145132)
      Zeder, M. A. Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proc. Natl. Acad. Sci. 105, 11597–11604, https://doi.org/10.1073/pnas.0801317105 (2008). (PMID: 10.1073/pnas.080131710518697943)
      Zeder, M. A. Animal domestication in the Zagros: a review of past and current research. Paléorient 25, 11–25, http://www.jstor.org/stable/41496540 (1999). (PMID: 10.3406/paleo.1999.4684)
      Zeder, M. A. & Hesse, B. The initial domestication of goats (Capra hircus) in the Zagros Mountains 10,000 years ago. Science 287, 2254–2257, https://doi.org/10.1126/science.287.5461.2254 (2000). (PMID: 10.1126/science.287.5461.225410731145)
      Pereira, F. & Amorim, A. Origin and spread of goat pastoralism. e LS; https://doi.org/10.1002/9780470015902.a0022864 (2001).
      Zeder, M. A. Out of the Fertile Crescent: The dispersal of domestic livestock through Europe and Africa in Hum. Dispersal Species Mov. From Prehistory to Present (ed. Boivin, N., Crassard, R. & Petraglia, M.) 261–296 (Cambridge University Press, 2017).
      Vigne, J. D. Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia since the last ice age. Mamm. Rev. 22, 87–96, https://doi.org/10.1111/j.1365-2907.1992.tb00124.x (1992). (PMID: 10.1111/j.1365-2907.1992.tb00124.x)
      Greenfield, H. J. et al. The origins of milk and wool production in the Old World: a zooarchaeological perspective from the Central Balkans [and comments]. Curr. Anthropol. 29, 573–593 (1988). (PMID: 10.1086/203676)
      Kaewthamasorn, M. et al. Genetic homogeneity of goat malaria parasites in Asia and Africa suggests their expansion with domestic goat host. Sci. Rep. 8, 5827, https://doi.org/10.1038/s41598-018-24048-0 (2018). (PMID: 10.1038/s41598-018-24048-0296434345895593)
      Mühlemann, B. et al. Ancient human parvovirus B19 in Eurasia reveals its long-term association with humans. Proc. Natl. Acad. Sci. 115, 7557–7562, https://doi.org/10.1073/pnas.1804921115 (2018). (PMID: 10.1073/pnas.180492111529967156)
      Otchere, I. D. et al. Comparative genomics of Mycobacterium africanum Lineage 5 and Lineage 6 from Ghana suggests distinct ecological niches. Sci. Rep. 8, 11269, https://doi.org/10.1038/s41598-018-29620-2 (2018). (PMID: 10.1038/s41598-018-29620-2300501666062541)
      Sigurdsson, B., Grímsson, H. & Pálsson, P. A. Maedi, a chronic, progressive infection of sheep’s lungs. J. Infect. Dis. 90, 233–241 (1952). (PMID: 10.1093/infdis/90.3.233)
      Blacklaws, B. A. et al. Transmission of small ruminant lentiviruses. Vet. Microbiol. 101, 199–208, https://doi.org/10.1016/j.vetmic.2004.04.006 (2004). (PMID: 10.1016/j.vetmic.2004.04.00615223124)
      Thormar, H. The origin of lentivirus research: Maedi-visna virus. Curr. HIV Res. 11, 2–9, https://doi.org/10.2174/157016213804999212 (2013). (PMID: 10.2174/15701621380499921223278353)
      Straub, O. C. Maedi–Visna virus infection in sheep. History and present knowledge. Comp. Immunol. Microbiol. Infect. Dis. 27, 1–5, https://doi.org/10.1016/S0147-9571(02)00078-4 (2004). (PMID: 10.1016/S0147-9571(02)00078-414656537)
      Sayari, M. & Soltanian, S. Serological and pathological study of Maedi-like diseases in mammary glands of sheep of Ahwaz region. Pajouhesh Sazandegi (in Persian), 2–7 (2001).
      Azizi, S. et al. Maedi in slaughtered sheep: A pathology and polymerase chain reaction study in southwestern Iran. Trop. Anim. Health Prod. 44, 113–118, https://doi.org/10.1007/s11250-011-9896-z (2012). (PMID: 10.1007/s11250-011-9896-z21643662)
      Norouzi, B., Razavizadeh, A. T., Azizzadeh, M., Mayameei, A. & Mashhadi, V. N. N. Serological study of small ruminant lentiviruses in sheep population of Khorasan-e-Razavi province in Iran. Veterinary Research Forum, 6, 245–249, PMC4611980 (2015).
      Sasani, F., Javanbakht, J., Hemmatzadeh, F., Moghadam, M. R. & Hassan, M. A. M. Evaluation of histopathological on maedi disease with serological confirmation in North-East of Iran. Res. J. Infect. Dis. 1, 5, https://doi.org/10.7243/2052-5958-1-5 (2013). (PMID: 10.7243/2052-5958-1-5)
      Molaee, V., Otarod, V., Abdollahi, D. & Lühken, G. Lentivirus susceptibility in Iranian and German sheep assessed by determination of TMEM154 E35K. Animals. 9, 685, https://doi.org/10.3390/ani9090685 (2019). (PMID: 10.3390/ani9090685)
      Alberto, F. J. et al. Convergent genomic signatures of domestication in sheep and goats. Nat. Commun. 9, 813, https://doi.org/10.1038/s41467-018-03206-y (2018). (PMID: 10.1038/s41467-018-03206-y295111745840369)
      L’Homme, Y. et al. Molecular characterization and phylogenetic analysis of small ruminant lentiviruses isolated from Canadian sheep and goats. Virol. J. 8, 271, https://doi.org/10.1186/1743-422X-8-271 (2011). (PMID: 10.1186/1743-422X-8-271216399043123287)
      Molaee, V., Eltanany, M. & Lühken, G. First survey on association of TMEM154 and CCR5 variants with serological maedi-visna status of sheep in German flocks. Vet. Res. 49, 36, https://doi.org/10.1186/s13567-018-0533-y (2018). (PMID: 10.1186/s13567-018-0533-y296733995909245)
      Muz, D. et al. First molecular characterization of visna/maedi viruses from naturally infected sheep in Turkey. Arch. Virol. 158, 559–570, https://doi.org/10.1007/s00705-012-1518-1 (2013). (PMID: 10.1007/s00705-012-1518-123124887)
      Hiendleder, S., Mainz, K., Plante, Y. & Lewalski, H. Analysis of mitochondrial DNA indicates that domestic sheep are derived from two different ancestral maternal sources: no evidence for contributions from urial and argali sheep. J. Hered. 89, 113–120, https://doi.org/10.1093/jhered/89.2.113 (1998). (PMID: 10.1093/jhered/89.2.1139542158)
      Hiendleder, S., Kaupe, B., Wassmuth, R. & Janke, A. Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proc. R. Soc. London. Ser. B Biol. Sci. 269, 893–904, https://doi.org/10.1098/rspb.2002.1975 (2002). (PMID: 10.1098/rspb.2002.1975)
      Pedrosa, S. et al. Evidence of three maternal lineages in Near Eastern sheep supporting multiple domestication events. Proc. R. Soc. B Biol. Sci. 272, 2211–2217, https://doi.org/10.1098/rspb.2005.3204 (2005). (PMID: 10.1098/rspb.2005.3204)
      Meadows, J. R. S., Cemal, I., Karaca, O., Gootwine, E. & Kijas, J. W. Five ovine mitochondrial lineages identified from sheep breeds of the near East. Genetics 175, 1371–1379, https://doi.org/10.1534/genetics.106.068353 (2007). (PMID: 10.1534/genetics.106.068353171947731840082)
      Meadows, J. R. S., Hiendleder, S. & Kijas, J. W. Haplogroup relationships between domestic and wild sheep resolved using a mitogenome panel. Heredity (Edinb). 106, 700, https://doi.org/10.1038/hdy.2010.122 (2011). (PMID: 10.1038/hdy.2010.12220940734)
      Bruford, M. W., Bradley, D. G. & Luikart, G. DNA markers reveal the complexity of livestock domestication. Nat. Rev. Genet. 4, 900, https://doi.org/10.1038/nrg1203 (2003). (PMID: 10.1038/nrg120314634637)
      Harlan, J. R. & Zohary, D. Distribution of wild wheats and barley. Science. 153, 1074–1080, https://doi.org/10.1126/science.153.3740.1074 (1966). (PMID: 10.1126/science.153.3740.107417737582)
      Sunderman, F. & Johns, M. Awassi fat tails: a chance for premium exports. J. Dep. Agric. West. Aust. Ser. 4 35, 99–105 (1994).
      Martin, D. P., Murrell, B., Golden, M., Khoosal, A. & Muhire, B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol., 1; https://doi.org/10.1093/ve/vev003 (2015).
      Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874, https://doi.org/10.1093/molbev/msw054 (2016). (PMID: 10.1093/molbev/msw0542700490427004904)
      Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526, https://doi.org/10.1093/oxfordjournals.molbev.a040023 (1993). (PMID: 10.1093/oxfordjournals.molbev.a0400238336541)
      Staskus, K. A. et al. Isolation of replication-competent molecular clones of visna virus. Virology 181, 228–240, https://doi.org/10.1016/0042-6822(91)90488-W (1991). (PMID: 10.1016/0042-6822(91)90488-W1847257)
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      Date Created: 20200212 Date Completed: 20201111 Latest Revision: 20210209
    • Publication Date:
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    • Accession Number:
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