Provenance and Geographic Spread of St. Louis Encephalitis Virus

ABSTRACT St. Louis encephalitis virus (SLEV) is the prototypic mosquito-borne flavivirus in the Americas. Birds are its primary vertebrate hosts, but amplification in certain mammals has also been suggested. The place and time of SLEV emergence remain unknown. In an ecological investigation in a tro...

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Autores principales: Anne Kopp, Thomas R. Gillespie, Daniel Hobelsberger, Alejandro Estrada, James M. Harper, Richard A. Miller, Isabella Eckerle, Marcel A. Müller, Lars Podsiadlowski, Fabian H. Leendertz, Christian Drosten, Sandra Junglen
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Publicado: American Society for Microbiology 2013
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spelling oai:doaj.org-article:5e3aeefdfd3348ca88dcd3ace89d04892021-11-15T15:40:05ZProvenance and Geographic Spread of St. Louis Encephalitis Virus10.1128/mBio.00322-132150-7511https://doaj.org/article/5e3aeefdfd3348ca88dcd3ace89d04892013-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00322-13https://doaj.org/toc/2150-7511ABSTRACT St. Louis encephalitis virus (SLEV) is the prototypic mosquito-borne flavivirus in the Americas. Birds are its primary vertebrate hosts, but amplification in certain mammals has also been suggested. The place and time of SLEV emergence remain unknown. In an ecological investigation in a tropical rainforest in Palenque National Park, Mexico, we discovered an ancestral variant of SLEV in Culex nigripalpus mosquitoes. Those SLEV-Palenque strains form a highly distinct phylogenetic clade within the SLEV species. Cell culture studies of SLEV-Palenque versus epidemic SLEV (MSI-7) revealed no growth differences in insect cells but a clear inability of SLEV-Palenque to replicate in cells from birds, cotton rats, and free-tailed bats permissive for MSI-7 replication. Only cells from nonhuman primates and neotropical fruit bats were moderately permissive. Phylogeographic reconstruction identified the common ancestor of all epidemic SLEV strains to have existed in an area between southern Mexico and Panama ca. 330 years ago. Expansion of the epidemic lineage occurred in two waves, the first representing emergence near the area of origin and the second involving almost parallel appearances of the virus in the lower Mississippi and Amazon delta regions. Early diversification events overlapped human habitat invasion during the post-Columbian era. Several documented SLEV outbreaks, such as the 1964 Houston epidemic or the 1990 Tampa epidemic, were predated by the arrival of novel strains between 1 and 4 years before the outbreaks. Collectively, our data provide insight into the putative origins of SLEV, suggesting that virus emergence was driven by human invasion of primary rainforests. IMPORTANCE St. Louis encephalitis virus (SLEV) is the prototypic mosquito-transmitted flavivirus of the Americas. Unlike the West Nile virus, which we know was recently introduced into North America from the Old World, the provenience of SLEV is obscure. In an ecological investigation in a primary rainforest area of Palenque National Park, Mexico, we have discovered an ancestral variant of SLEV. The ancestral virus was much less active than the epidemic virus in cell cultures, reflecting its incomplete adaptation to hosts encountered outside primary rainforests. Knowledge of this virus enabled a spatiotemporal reconstruction of the common ancestor of all SLEVs and how the virus spread from there. We can infer that the cosmopolitan SLEV lineage emerged from Central America in the 17th century, a period of post-Columbian colonial history marked by intense human invasion of primary rainforests. Further spread followed major bird migration pathways over North and South America.Anne KoppThomas R. GillespieDaniel HobelsbergerAlejandro EstradaJames M. HarperRichard A. MillerIsabella EckerleMarcel A. MüllerLars PodsiadlowskiFabian H. LeendertzChristian DrostenSandra JunglenAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 3 (2013)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Anne Kopp
Thomas R. Gillespie
Daniel Hobelsberger
Alejandro Estrada
James M. Harper
Richard A. Miller
Isabella Eckerle
Marcel A. Müller
Lars Podsiadlowski
Fabian H. Leendertz
Christian Drosten
Sandra Junglen
Provenance and Geographic Spread of St. Louis Encephalitis Virus
description ABSTRACT St. Louis encephalitis virus (SLEV) is the prototypic mosquito-borne flavivirus in the Americas. Birds are its primary vertebrate hosts, but amplification in certain mammals has also been suggested. The place and time of SLEV emergence remain unknown. In an ecological investigation in a tropical rainforest in Palenque National Park, Mexico, we discovered an ancestral variant of SLEV in Culex nigripalpus mosquitoes. Those SLEV-Palenque strains form a highly distinct phylogenetic clade within the SLEV species. Cell culture studies of SLEV-Palenque versus epidemic SLEV (MSI-7) revealed no growth differences in insect cells but a clear inability of SLEV-Palenque to replicate in cells from birds, cotton rats, and free-tailed bats permissive for MSI-7 replication. Only cells from nonhuman primates and neotropical fruit bats were moderately permissive. Phylogeographic reconstruction identified the common ancestor of all epidemic SLEV strains to have existed in an area between southern Mexico and Panama ca. 330 years ago. Expansion of the epidemic lineage occurred in two waves, the first representing emergence near the area of origin and the second involving almost parallel appearances of the virus in the lower Mississippi and Amazon delta regions. Early diversification events overlapped human habitat invasion during the post-Columbian era. Several documented SLEV outbreaks, such as the 1964 Houston epidemic or the 1990 Tampa epidemic, were predated by the arrival of novel strains between 1 and 4 years before the outbreaks. Collectively, our data provide insight into the putative origins of SLEV, suggesting that virus emergence was driven by human invasion of primary rainforests. IMPORTANCE St. Louis encephalitis virus (SLEV) is the prototypic mosquito-transmitted flavivirus of the Americas. Unlike the West Nile virus, which we know was recently introduced into North America from the Old World, the provenience of SLEV is obscure. In an ecological investigation in a primary rainforest area of Palenque National Park, Mexico, we have discovered an ancestral variant of SLEV. The ancestral virus was much less active than the epidemic virus in cell cultures, reflecting its incomplete adaptation to hosts encountered outside primary rainforests. Knowledge of this virus enabled a spatiotemporal reconstruction of the common ancestor of all SLEVs and how the virus spread from there. We can infer that the cosmopolitan SLEV lineage emerged from Central America in the 17th century, a period of post-Columbian colonial history marked by intense human invasion of primary rainforests. Further spread followed major bird migration pathways over North and South America.
format article
author Anne Kopp
Thomas R. Gillespie
Daniel Hobelsberger
Alejandro Estrada
James M. Harper
Richard A. Miller
Isabella Eckerle
Marcel A. Müller
Lars Podsiadlowski
Fabian H. Leendertz
Christian Drosten
Sandra Junglen
author_facet Anne Kopp
Thomas R. Gillespie
Daniel Hobelsberger
Alejandro Estrada
James M. Harper
Richard A. Miller
Isabella Eckerle
Marcel A. Müller
Lars Podsiadlowski
Fabian H. Leendertz
Christian Drosten
Sandra Junglen
author_sort Anne Kopp
title Provenance and Geographic Spread of St. Louis Encephalitis Virus
title_short Provenance and Geographic Spread of St. Louis Encephalitis Virus
title_full Provenance and Geographic Spread of St. Louis Encephalitis Virus
title_fullStr Provenance and Geographic Spread of St. Louis Encephalitis Virus
title_full_unstemmed Provenance and Geographic Spread of St. Louis Encephalitis Virus
title_sort provenance and geographic spread of st. louis encephalitis virus
publisher American Society for Microbiology
publishDate 2013
url https://doaj.org/article/5e3aeefdfd3348ca88dcd3ace89d0489
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