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Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses
Until recently, hantaviruses (family Bunyaviridae) were believed to originate from rodent reservoirs. However, genetically distinct hantaviruses were lately found in shrews and moles, as well as in bats from Africa and Asia. Bats (order Chiroptera) are considered important reservoir hosts for emergi...
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Published in: | Infection, genetics and evolution genetics and evolution, 2016-07, Vol.41, p.113-119 |
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creator | Witkowski, Peter T. Drexler, Jan F. Kallies, René Ličková, Martina Bokorová, Silvia Mananga, Gael D. Szemes, Tomáš Leroy, Eric M. Krüger, Detlev H. Drosten, Christian Klempa, Boris |
description | Until recently, hantaviruses (family Bunyaviridae) were believed to originate from rodent reservoirs. However, genetically distinct hantaviruses were lately found in shrews and moles, as well as in bats from Africa and Asia. Bats (order Chiroptera) are considered important reservoir hosts for emerging human pathogens. Here, we report on the identification of a novel hantavirus, provisionally named Makokou virus (MAKV), in Noack's Roundleaf Bat (Hipposideros ruber) in Gabon, Central Africa. Phylogenetic analysis of the genomic l-segment showed that MAKV was the most closely related to other bat-borne hantaviruses and shared a most recent common ancestor with the Asian hantaviruses Xuan Son and Laibin. Breakdown of the virus load in a bat animal showed that MAKV resembles rodent-borne hantaviruses in its organ distribution in that it predominantly occurred in the spleen and kidney; this provides a first insight into the infection pattern of bat-borne hantaviruses. Ancestral state reconstruction based on a tree of l gene sequences of all relevant hantavirus lineages was combined with phylogenetic fossil host hypothesis testing, leading to a statistically significant rejection of the mammalian superorder Euarchontoglires (including rodents) but not the superorder Laurasiatheria (including shrews, moles, and bats) as potential hosts of ancestral hantaviruses at most basal tree nodes. Our data supports the emerging concept of bats as previously overlooked hantavirus reservoir hosts.
•Novel tentative Hantavirus species (Makokou virus) in Hipposideros bat from Gabon•MAKV phylogenetically groups with novel hantaviruses from shrews, moles, and bats•Virus load in H. ruber resembles organ distribution usually found in rodent hosts.•Laurasiatheria are the most probable host ancestor for the genus Hantavirus. |
doi_str_mv | 10.1016/j.meegid.2016.03.036 |
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•Novel tentative Hantavirus species (Makokou virus) in Hipposideros bat from Gabon•MAKV phylogenetically groups with novel hantaviruses from shrews, moles, and bats•Virus load in H. ruber resembles organ distribution usually found in rodent hosts.•Laurasiatheria are the most probable host ancestor for the genus Hantavirus.</description><identifier>ISSN: 1567-1348</identifier><identifier>EISSN: 1567-7257</identifier><identifier>DOI: 10.1016/j.meegid.2016.03.036</identifier><identifier>PMID: 27051047</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Africa ; Animals ; Bat ; Biological Evolution ; Caves ; Chiroptera - virology ; Disease Reservoirs ; Gabon - epidemiology ; Hantavirus ; Hantavirus - classification ; Hantavirus - genetics ; Hantavirus - isolation & purification ; Hantavirus Infections - epidemiology ; Hantavirus Infections - veterinary ; Hantavirus Infections - virology ; Kidney - virology ; Laurasiatheria ; Makokou virus ; Mammals ; Organ Specificity ; Phylogeny ; Reverse Transcriptase Polymerase Chain Reaction ; RNA, Viral - genetics ; Sequence Analysis, DNA ; Spleen - virology ; Viral Load ; Zoonosis</subject><ispartof>Infection, genetics and evolution, 2016-07, Vol.41, p.113-119</ispartof><rights>2016 Elsevier B.V.</rights><rights>Copyright © 2016 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c428t-12f0c4b84ef2573b68613124bee6811c1ce11ea16fa3d476a533d982458340e93</citedby><cites>FETCH-LOGICAL-c428t-12f0c4b84ef2573b68613124bee6811c1ce11ea16fa3d476a533d982458340e93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,778,782,27911,27912</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27051047$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Witkowski, Peter T.</creatorcontrib><creatorcontrib>Drexler, Jan F.</creatorcontrib><creatorcontrib>Kallies, René</creatorcontrib><creatorcontrib>Ličková, Martina</creatorcontrib><creatorcontrib>Bokorová, Silvia</creatorcontrib><creatorcontrib>Mananga, Gael D.</creatorcontrib><creatorcontrib>Szemes, Tomáš</creatorcontrib><creatorcontrib>Leroy, Eric M.</creatorcontrib><creatorcontrib>Krüger, Detlev H.</creatorcontrib><creatorcontrib>Drosten, Christian</creatorcontrib><creatorcontrib>Klempa, Boris</creatorcontrib><title>Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses</title><title>Infection, genetics and evolution</title><addtitle>Infect Genet Evol</addtitle><description>Until recently, hantaviruses (family Bunyaviridae) were believed to originate from rodent reservoirs. However, genetically distinct hantaviruses were lately found in shrews and moles, as well as in bats from Africa and Asia. Bats (order Chiroptera) are considered important reservoir hosts for emerging human pathogens. Here, we report on the identification of a novel hantavirus, provisionally named Makokou virus (MAKV), in Noack's Roundleaf Bat (Hipposideros ruber) in Gabon, Central Africa. Phylogenetic analysis of the genomic l-segment showed that MAKV was the most closely related to other bat-borne hantaviruses and shared a most recent common ancestor with the Asian hantaviruses Xuan Son and Laibin. Breakdown of the virus load in a bat animal showed that MAKV resembles rodent-borne hantaviruses in its organ distribution in that it predominantly occurred in the spleen and kidney; this provides a first insight into the infection pattern of bat-borne hantaviruses. Ancestral state reconstruction based on a tree of l gene sequences of all relevant hantavirus lineages was combined with phylogenetic fossil host hypothesis testing, leading to a statistically significant rejection of the mammalian superorder Euarchontoglires (including rodents) but not the superorder Laurasiatheria (including shrews, moles, and bats) as potential hosts of ancestral hantaviruses at most basal tree nodes. Our data supports the emerging concept of bats as previously overlooked hantavirus reservoir hosts.
•Novel tentative Hantavirus species (Makokou virus) in Hipposideros bat from Gabon•MAKV phylogenetically groups with novel hantaviruses from shrews, moles, and bats•Virus load in H. ruber resembles organ distribution usually found in rodent hosts.•Laurasiatheria are the most probable host ancestor for the genus Hantavirus.</description><subject>Africa</subject><subject>Animals</subject><subject>Bat</subject><subject>Biological Evolution</subject><subject>Caves</subject><subject>Chiroptera - virology</subject><subject>Disease Reservoirs</subject><subject>Gabon - epidemiology</subject><subject>Hantavirus</subject><subject>Hantavirus - classification</subject><subject>Hantavirus - genetics</subject><subject>Hantavirus - isolation & purification</subject><subject>Hantavirus Infections - epidemiology</subject><subject>Hantavirus Infections - veterinary</subject><subject>Hantavirus Infections - virology</subject><subject>Kidney - virology</subject><subject>Laurasiatheria</subject><subject>Makokou virus</subject><subject>Mammals</subject><subject>Organ Specificity</subject><subject>Phylogeny</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>RNA, Viral - genetics</subject><subject>Sequence Analysis, DNA</subject><subject>Spleen - virology</subject><subject>Viral Load</subject><subject>Zoonosis</subject><issn>1567-1348</issn><issn>1567-7257</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNp9kc-KFDEQxoMo7rr6BiI5eukx6aSTzEWQZf0DC3rQc6hOV-9k6E7GVPfKPIJvbdYZ9ygUJBV-9VWqPsZeS7GRQpp3-82MeBeHTVuzjVA1zBN2KTtjG9t29un5LpV2F-wF0V4IaUXrnrOL1opOCm0v2e9vu-OU7zDhEgOHBNORIvE8cuAJf415TQPvYWn6XBLyHaQF7mNZidN6OOSyUAUnWAtQhGWHJULiu0wLB6Ic6lvMiY-5VO2AtBSY-AzzDNNf8FEO6SV7NsJE-Op8XrEfH2--X39ubr9--nL94bYJunVLI9tRBN07jWMdUvXGGalkq3tE46QMMqCUCNKMoAZtDXRKDVvX6s4pLXCrrtjbk-6h5J9r_ZKfIwWcJkiYV_LSuq3eWmdtRfUJDSUTFRz9ocQZytFL4R9M8Ht_MsE_mOCFqmFq2Ztzh7WfcXgs-rf1Crw_AVjnvI9YPIWIdT9DLBgWP-T4_w5_AIj8nWY</recordid><startdate>201607</startdate><enddate>201607</enddate><creator>Witkowski, Peter T.</creator><creator>Drexler, Jan F.</creator><creator>Kallies, René</creator><creator>Ličková, Martina</creator><creator>Bokorová, Silvia</creator><creator>Mananga, Gael D.</creator><creator>Szemes, Tomáš</creator><creator>Leroy, Eric M.</creator><creator>Krüger, Detlev H.</creator><creator>Drosten, Christian</creator><creator>Klempa, Boris</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>201607</creationdate><title>Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses</title><author>Witkowski, Peter T. ; Drexler, Jan F. ; Kallies, René ; Ličková, Martina ; Bokorová, Silvia ; Mananga, Gael D. ; Szemes, Tomáš ; Leroy, Eric M. ; Krüger, Detlev H. ; Drosten, Christian ; Klempa, Boris</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c428t-12f0c4b84ef2573b68613124bee6811c1ce11ea16fa3d476a533d982458340e93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Africa</topic><topic>Animals</topic><topic>Bat</topic><topic>Biological Evolution</topic><topic>Caves</topic><topic>Chiroptera - virology</topic><topic>Disease Reservoirs</topic><topic>Gabon - epidemiology</topic><topic>Hantavirus</topic><topic>Hantavirus - classification</topic><topic>Hantavirus - genetics</topic><topic>Hantavirus - isolation & purification</topic><topic>Hantavirus Infections - epidemiology</topic><topic>Hantavirus Infections - veterinary</topic><topic>Hantavirus Infections - virology</topic><topic>Kidney - virology</topic><topic>Laurasiatheria</topic><topic>Makokou virus</topic><topic>Mammals</topic><topic>Organ Specificity</topic><topic>Phylogeny</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>RNA, Viral - genetics</topic><topic>Sequence Analysis, DNA</topic><topic>Spleen - virology</topic><topic>Viral Load</topic><topic>Zoonosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Witkowski, Peter T.</creatorcontrib><creatorcontrib>Drexler, Jan F.</creatorcontrib><creatorcontrib>Kallies, René</creatorcontrib><creatorcontrib>Ličková, Martina</creatorcontrib><creatorcontrib>Bokorová, Silvia</creatorcontrib><creatorcontrib>Mananga, Gael D.</creatorcontrib><creatorcontrib>Szemes, Tomáš</creatorcontrib><creatorcontrib>Leroy, Eric M.</creatorcontrib><creatorcontrib>Krüger, Detlev H.</creatorcontrib><creatorcontrib>Drosten, Christian</creatorcontrib><creatorcontrib>Klempa, Boris</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Infection, genetics and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Witkowski, Peter T.</au><au>Drexler, Jan F.</au><au>Kallies, René</au><au>Ličková, Martina</au><au>Bokorová, Silvia</au><au>Mananga, Gael D.</au><au>Szemes, Tomáš</au><au>Leroy, Eric M.</au><au>Krüger, Detlev H.</au><au>Drosten, Christian</au><au>Klempa, Boris</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses</atitle><jtitle>Infection, genetics and evolution</jtitle><addtitle>Infect Genet Evol</addtitle><date>2016-07</date><risdate>2016</risdate><volume>41</volume><spage>113</spage><epage>119</epage><pages>113-119</pages><issn>1567-1348</issn><eissn>1567-7257</eissn><abstract>Until recently, hantaviruses (family Bunyaviridae) were believed to originate from rodent reservoirs. However, genetically distinct hantaviruses were lately found in shrews and moles, as well as in bats from Africa and Asia. Bats (order Chiroptera) are considered important reservoir hosts for emerging human pathogens. Here, we report on the identification of a novel hantavirus, provisionally named Makokou virus (MAKV), in Noack's Roundleaf Bat (Hipposideros ruber) in Gabon, Central Africa. Phylogenetic analysis of the genomic l-segment showed that MAKV was the most closely related to other bat-borne hantaviruses and shared a most recent common ancestor with the Asian hantaviruses Xuan Son and Laibin. Breakdown of the virus load in a bat animal showed that MAKV resembles rodent-borne hantaviruses in its organ distribution in that it predominantly occurred in the spleen and kidney; this provides a first insight into the infection pattern of bat-borne hantaviruses. Ancestral state reconstruction based on a tree of l gene sequences of all relevant hantavirus lineages was combined with phylogenetic fossil host hypothesis testing, leading to a statistically significant rejection of the mammalian superorder Euarchontoglires (including rodents) but not the superorder Laurasiatheria (including shrews, moles, and bats) as potential hosts of ancestral hantaviruses at most basal tree nodes. Our data supports the emerging concept of bats as previously overlooked hantavirus reservoir hosts.
•Novel tentative Hantavirus species (Makokou virus) in Hipposideros bat from Gabon•MAKV phylogenetically groups with novel hantaviruses from shrews, moles, and bats•Virus load in H. ruber resembles organ distribution usually found in rodent hosts.•Laurasiatheria are the most probable host ancestor for the genus Hantavirus.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>27051047</pmid><doi>10.1016/j.meegid.2016.03.036</doi><tpages>7</tpages></addata></record> |
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subjects | Africa Animals Bat Biological Evolution Caves Chiroptera - virology Disease Reservoirs Gabon - epidemiology Hantavirus Hantavirus - classification Hantavirus - genetics Hantavirus - isolation & purification Hantavirus Infections - epidemiology Hantavirus Infections - veterinary Hantavirus Infections - virology Kidney - virology Laurasiatheria Makokou virus Mammals Organ Specificity Phylogeny Reverse Transcriptase Polymerase Chain Reaction RNA, Viral - genetics Sequence Analysis, DNA Spleen - virology Viral Load Zoonosis |
title | Phylogenetic analysis of a newfound bat-borne hantavirus supports a laurasiatherian host association for ancestral mammalian hantaviruses |
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