Modern-day SIV viral diversity generated by extensive recombination and cross-species transmission
Identifieur interne : 001104 ( Pmc/Curation ); précédent : 001103; suivant : 001105Modern-day SIV viral diversity generated by extensive recombination and cross-species transmission
Auteurs : Sidney M. Bell [États-Unis] ; Trevor Bedford [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2017.
Abstract
Cross-species transmission (CST) has led to many devastating epidemics, but is still a poorly understood phenomenon. HIV-1 and HIV-2 (human immunodeficiency virus 1 and 2), which have collectively caused over 35 million deaths, are the result of multiple CSTs from chimpanzees, gorillas, and sooty mangabeys. While the immediate history of HIV is known, there are over 45 lentiviruses that infect specific species of primates, and patterns of host switching are not well characterized. We thus took a phylogenetic approach to better understand the natural history of SIV recombination and CST. We modeled host species as a discrete character trait on the viral phylogeny and inferred historical host switches and the pairwise transmission rates between each pair of 24 primate hosts. We identify 14 novel, well-supported, ancient cross-species transmission events. We also find that lentiviral lineages vary widely in their ability to infect new host species: SIV
Url:
DOI: 10.1371/journal.ppat.1006466
PubMed: 28672035
PubMed Central: 5510905
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<front><div type="abstract" xml:lang="en"><p>Cross-species transmission (CST) has led to many devastating epidemics, but is still a poorly understood phenomenon. HIV-1 and HIV-2 (human immunodeficiency virus 1 and 2), which have collectively caused over 35 million deaths, are the result of multiple CSTs from chimpanzees, gorillas, and sooty mangabeys. While the immediate history of HIV is known, there are over 45 lentiviruses that infect specific species of primates, and patterns of host switching are not well characterized. We thus took a phylogenetic approach to better understand the natural history of SIV recombination and CST. We modeled host species as a discrete character trait on the viral phylogeny and inferred historical host switches and the pairwise transmission rates between each pair of 24 primate hosts. We identify 14 novel, well-supported, ancient cross-species transmission events. We also find that lentiviral lineages vary widely in their ability to infect new host species: SIV<italic>col</italic>
(from colobus monkeys) is evolutionarily isolated, while SIV<italic>agm</italic>
s (from African green monkeys) frequently move between host subspecies. We also examine the origins of SIV<italic>cpz</italic>
(the predecessor of HIV-1) in greater detail than previous studies, and find that there are still large portions of the genome with unknown origins. Observed patterns of CST are likely driven by a combination of ecological circumstance and innate immune factors.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plospath</journal-id>
<journal-title-group><journal-title>PLoS Pathogens</journal-title>
</journal-title-group>
<issn pub-type="ppub">1553-7366</issn>
<issn pub-type="epub">1553-7374</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">28672035</article-id>
<article-id pub-id-type="pmc">5510905</article-id>
<article-id pub-id-type="doi">10.1371/journal.ppat.1006466</article-id>
<article-id pub-id-type="publisher-id">PPATHOGENS-D-17-00122</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Phylogenetic Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Phylogenetic Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Computer and Information Sciences</subject>
<subj-group><subject>Data Management</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Phylogenetic Analysis</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Animals</subject>
<subj-group><subject>Vertebrates</subject>
<subj-group><subject>Amniotes</subject>
<subj-group><subject>Mammals</subject>
<subj-group><subject>Primates</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Medical Microbiology</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Immunodeficiency Viruses</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Pathology and Laboratory Medicine</subject>
<subj-group><subject>Pathogens</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Immunodeficiency Viruses</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Immunodeficiency Viruses</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>Immunodeficiency Viruses</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>RNA viruses</subject>
<subj-group><subject>Retroviruses</subject>
<subj-group><subject>Lentivirus</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Medical Microbiology</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Retroviruses</subject>
<subj-group><subject>Lentivirus</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject>
<subj-group><subject>Pathology and Laboratory Medicine</subject>
<subj-group><subject>Pathogens</subject>
<subj-group><subject>Microbial Pathogens</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Retroviruses</subject>
<subj-group><subject>Lentivirus</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Viruses</subject>
<subj-group><subject>Viral Pathogens</subject>
<subj-group><subject>Retroviruses</subject>
<subj-group><subject>Lentivirus</subject>
<subj-group><subject>SIV</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Genetics</subject>
<subj-group><subject>Genomics</subject>
<subj-group><subject>Animal Genomics</subject>
<subj-group><subject>Mammalian Genomics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Animal Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Animal Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Computer and Information Sciences</subject>
<subj-group><subject>Data Management</subject>
<subj-group><subject>Taxonomy</subject>
<subj-group><subject>Evolutionary Systematics</subject>
<subj-group><subject>Phylogenetics</subject>
<subj-group><subject>Animal Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Zoology</subject>
<subj-group><subject>Animal Phylogenetics</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Organisms</subject>
<subj-group><subject>Animals</subject>
<subj-group><subject>Vertebrates</subject>
<subj-group><subject>Amniotes</subject>
<subj-group><subject>Mammals</subject>
<subj-group><subject>Primates</subject>
<subj-group><subject>Monkeys</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Microbial Evolution</subject>
<subj-group><subject>Viral Evolution</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Evolutionary Biology</subject>
<subj-group><subject>Organismal Evolution</subject>
<subj-group><subject>Microbial Evolution</subject>
<subj-group><subject>Viral Evolution</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Microbiology</subject>
<subj-group><subject>Virology</subject>
<subj-group><subject>Viral Evolution</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Database and Informatics Methods</subject>
<subj-group><subject>Bioinformatics</subject>
<subj-group><subject>Sequence Analysis</subject>
<subj-group><subject>Sequence Alignment</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Modern-day SIV viral diversity generated by extensive recombination and cross-species transmission</article-title>
<alt-title alt-title-type="running-head">SIV diversity generated by recombination, cross-species transmission</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1933-6033</contrib-id>
<name><surname>Bell</surname>
<given-names>Sidney M.</given-names>
</name>
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<role content-type="http://credit.casrai.org/">Data curation</role>
<role content-type="http://credit.casrai.org/">Formal analysis</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Investigation</role>
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<role content-type="http://credit.casrai.org/">Validation</role>
<role content-type="http://credit.casrai.org/">Visualization</role>
<role content-type="http://credit.casrai.org/">Writing – original draft</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bedford</surname>
<given-names>Trevor</given-names>
</name>
<role content-type="http://credit.casrai.org/">Conceptualization</role>
<role content-type="http://credit.casrai.org/">Funding acquisition</role>
<role content-type="http://credit.casrai.org/">Investigation</role>
<role content-type="http://credit.casrai.org/">Methodology</role>
<role content-type="http://credit.casrai.org/">Project administration</role>
<role content-type="http://credit.casrai.org/">Resources</role>
<role content-type="http://credit.casrai.org/">Supervision</role>
<role content-type="http://credit.casrai.org/">Validation</role>
<role content-type="http://credit.casrai.org/">Writing – review & editing</role>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Molecular and Cellular Biology Program, University of Washington, Seattle, Washington, United States of America</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Silvestri</surname>
<given-names>Guido</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Emory University, UNITED STATES</addr-line>
</aff>
<author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p>
</fn>
<corresp id="cor001">* E-mail: <email>sbell23@fredhutch.org</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>3</day>
<month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection"><month>7</month>
<year>2017</year>
</pub-date>
<volume>13</volume>
<issue>7</issue>
<elocation-id>e1006466</elocation-id>
<history><date date-type="received"><day>19</day>
<month>1</month>
<year>2017</year>
</date>
<date date-type="accepted"><day>12</day>
<month>6</month>
<year>2017</year>
</date>
</history>
<permissions><copyright-statement>© 2017 Bell, Bedford</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>Bell, Bedford</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="ppat.1006466.pdf"></self-uri>
<abstract><p>Cross-species transmission (CST) has led to many devastating epidemics, but is still a poorly understood phenomenon. HIV-1 and HIV-2 (human immunodeficiency virus 1 and 2), which have collectively caused over 35 million deaths, are the result of multiple CSTs from chimpanzees, gorillas, and sooty mangabeys. While the immediate history of HIV is known, there are over 45 lentiviruses that infect specific species of primates, and patterns of host switching are not well characterized. We thus took a phylogenetic approach to better understand the natural history of SIV recombination and CST. We modeled host species as a discrete character trait on the viral phylogeny and inferred historical host switches and the pairwise transmission rates between each pair of 24 primate hosts. We identify 14 novel, well-supported, ancient cross-species transmission events. We also find that lentiviral lineages vary widely in their ability to infect new host species: SIV<italic>col</italic>
(from colobus monkeys) is evolutionarily isolated, while SIV<italic>agm</italic>
s (from African green monkeys) frequently move between host subspecies. We also examine the origins of SIV<italic>cpz</italic>
(the predecessor of HIV-1) in greater detail than previous studies, and find that there are still large portions of the genome with unknown origins. Observed patterns of CST are likely driven by a combination of ecological circumstance and innate immune factors.</p>
</abstract>
<abstract abstract-type="summary"><title>Author summary</title>
<p>Virus cross-species transmissions (CSTs) can cause devastating epidemics, including EBOV, MERS, and HIV. HIV is actually one of over 45 similar viruses, called SIVs, which infect primates; the emergence of HIV as a human pathogen was the result of multiple CSTs, and yet it is not understood how commonly these viruses switch hosts. We used publicly available genetic sequence data to reconstruct the evolutionary history of these viruses. We found evidence for at least 13 instances of recombination between lineages of SIV, and identified at least 14 ancient cross-species transmission events where an SIV switched hosts. These results provide important ecological context to the HIV pandemic, suggesting that while SIV CST is relatively rare over evolutionary time, it is an important factor that has shaped SIV biology and evolution.</p>
</abstract>
<funding-group><funding-statement>TB is a Pew Biomedical Scholar and his work is supported by National Institutes of Health award R35 GM119774-01. SB is a National Science Foundation Graduate Research Fellow and her work is supported by grant DGE-1256082. Her work is also supported by a training grant from the National Cancer Institute of the National Institutes of Health, award number T32CA080416; a Vassar Fellowship for Graduate Study; and an ARCS foundation fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement>
</funding-group>
<counts><fig-count count="4"></fig-count>
<table-count count="0"></table-count>
<page-count count="21"></page-count>
</counts>
<custom-meta-group><custom-meta><meta-name>PLOS Publication Stage</meta-name>
<meta-value>vor-update-to-uncorrected-proof</meta-value>
</custom-meta>
<custom-meta><meta-name>Publication Update</meta-name>
<meta-value>2017-07-14</meta-value>
</custom-meta>
<custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All datasets, config files, documentation, and scripts used in this analysis or to generate figures are available publicly at <<ext-link ext-link-type="uri" xlink:href="https://github.com/blab/siv-cst">https://github.com/blab/siv-cst</ext-link>
>.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All datasets, config files, documentation, and scripts used in this analysis or to generate figures are available publicly at <<ext-link ext-link-type="uri" xlink:href="https://github.com/blab/siv-cst">https://github.com/blab/siv-cst</ext-link>
>.</p>
</notes>
</front>
</pmc>
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