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Cited by 191RNA and protein synthesis mechanismsMosquito-borne diseases and controlEvolution and Genetic Dynamics

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Virus-Host Coevolution: Common Patterns of Nucleotide Motif Usage in Flaviviridae and Their Hosts

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Lobo, Francisco P., Mota, Bruno E. F., Pena, Sérgio D. J., Azevedo, Vasco, Macedo, Andréa M., Tauch, Andreas, Machado, Carlos R., Franco, Glória R.·2009·PLoS ONE
DOI 10.1371/journal.pone.0006282PMC PMC2707012
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Abstract

Virus-host biological interaction is a continuous coevolutionary process involving both host immune system and viral escape mechanisms. Flaviviridae family is composed of fast evolving RNA viruses that infects vertebrate (mammals and birds) and/or invertebrate (ticks and mosquitoes) organisms. These host groups are very distinct life forms separated by a long evolutionary time, so lineage-specific anti-viral mechanisms are likely to have evolved. Flaviviridae viruses which infect a single host lineage would be subjected to specific host-induced pressures and, therefore, selected by them. In this work we compare the genomic evolutionary patterns of Flaviviridae viruses and their hosts in an attempt to uncover coevolutionary processes inducing common features in such disparate groups. Especially, we have analyzed dinucleotide and codon usage patterns in the coding regions of vertebrate and invertebrate organisms as well as in Flaviviridae viruses which specifically infect one or both host types. The two host groups posses very distinctive dinucleotide and codon usage patterns. A pronounced CpG under-representation was found in the vertebrate group, possibly induced by the methylation-deamination process, as well as a prominent TpA decrease. The invertebrate group displayed only a TpA frequency reduction bias. Flaviviridae viruses mimicked host nucleotide motif usage in a host-specific manner. Vertebrate-infecting viruses possessed under-representation of CpG and TpA, and insect-only viruses displayed only a TpA under-representation bias. Single-host Flaviviridae members which persistently infect mammals or insect hosts (Hepacivirus and insect-only Flavivirus, respectively) were found to posses a codon usage profile more similar to that of their hosts than to related Flaviviridae. We demonstrated that vertebrates and mosquitoes genomes are under very distinct lineage-specific constraints, and Flaviviridae viruses which specifically infect these lineages appear to be subject to the same evolutionary pressures that shaped their host coding regions, evidencing the lineage-specific coevolutionary processes between the viral and host groups.

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Figures

Figure 1 Phylogenetic relationships among Flaviviridae viruses. Phylogenetic trees were constructed with whole polyprotein sequences using the Neighbor-Joining method. Bootstrap values were calculated after 1000 replicates, and the consensus tree is shown. Flavivirus genus is highlighted in blue, Pestivirus is in green and Hepacivirus is in salmon. Flavivirus genus was further divided to reflect distinct viral host range, with insect-only viruses in orange, NKV in purple, mosquito-borne in yellow and tick-borne in red. Acronyms and names of the viruses are located in the “viral dataset” section.
Figure 1 Phylogenetic relationships among Flaviviridae viruses. Phylogenetic trees were constructed with whole polyprotein sequences using the Neighbor-Joining method. Bootstrap values were calculated after 1000 replicates, and the consensus tree is shown. Flavivirus genus is highlighted in blue, Pestivirus is in green and Hepacivirus is in salmon. Flavivirus genus was further divided to reflect distinct viral host range, with insect-only viruses in orange, NKV in purple, mosquito-borne in yellow and tick-borne in red. Acronyms and names of the viruses are located in the “viral dataset” section.CC BY · PubMed Central
Figure 2 Differential dinucleotide usage in Flaviviridae and their hosts. Dinucleotide odds ratio values were calculated for individual species as described in the “Dinucleotide Odds Ratio Calculation” section, and the mean values (±SD) for host and viral groups are plotted. Differentially represented dinucleotides are highlighted in red. Dashed lines indicate cutoffs values of 0.78–1.25. For every group, mean odds ratio values among all dinucleotides (±SD) were calculated and are at the right top in each graph.
Figure 2 Differential dinucleotide usage in Flaviviridae and their hosts. Dinucleotide odds ratio values were calculated for individual species as described in the “Dinucleotide Odds Ratio Calculation” section, and the mean values (±SD) for host and viral groups are plotted. Differentially represented dinucleotides are highlighted in red. Dashed lines indicate cutoffs values of 0.78–1.25. For every group, mean odds ratio values among all dinucleotides (±SD) were calculated and are at the right top in each graph.CC BY · PubMed Central
Figure 3 Relative Synonymous Codon Usage (RSCU) in Flaviviridae and their hosts. RSCU mean values (±SD) were calculated for each host and viral group as described in the “Relative Synonymous Codon Usage Calculation” section. Only groups of synonymous codon containing one codon with a dinucleotide found as differentially represented (CpG, TpA, TpG or CpA) and one codon without them are displayed to allow relative comparison. Each box represents a set of synonymous codons possessing such property. CpG-containing codons are highlighted in red, TpA-containing are in green, TpG-containing are in purple and CpA-containing are in blue. For every group, mean RSCU values among all codons (±SD) were calculated and are at the right top in each graph.
Figure 3 Relative Synonymous Codon Usage (RSCU) in Flaviviridae and their hosts. RSCU mean values (±SD) were calculated for each host and viral group as described in the “Relative Synonymous Codon Usage Calculation” section. Only groups of synonymous codon containing one codon with a dinucleotide found as differentially represented (CpG, TpA, TpG or CpA) and one codon without them are displayed to allow relative comparison. Each box represents a set of synonymous codons possessing such property. CpG-containing codons are highlighted in red, TpA-containing are in green, TpG-containing are in purple and CpA-containing are in blue. For every group, mean RSCU values among all codons (±SD) were calculated and are at the right top in each graph.CC BY · PubMed Central
Figure 4 Ordered list of codons in Flaviviridae and hosts groups by their mean RSCU values. Mean RSCU values were calculated for each host and viral group as defined in the “Relative Synonymous Codon Usage Calculation” section. The codons in each group are ordered from low to top by their mean RSCU values. CpG-containing codons are highlighted in red and TpA-containing are in green. Codons with RSCU values smaller than one are highlighted in grey.
Figure 4 Ordered list of codons in Flaviviridae and hosts groups by their mean RSCU values. Mean RSCU values were calculated for each host and viral group as defined in the “Relative Synonymous Codon Usage Calculation” section. The codons in each group are ordered from low to top by their mean RSCU values. CpG-containing codons are highlighted in red and TpA-containing are in green. Codons with RSCU values smaller than one are highlighted in grey.CC BY · PubMed Central
Figure 5 Hierarchical clustering of Flaviviridae viruses and their hosts based on codon usage likeness. RSCU values were calculated for codons with degeneracy greater than one for every organism, generating a matrix of N×M dimensions, being N the number of species and M the number of degenerated codons. Hierarchical clustering of organisms was conducted based on Spearman's rho correlation coefficients of RSCU values. Color schema for clusters is the same used in Figure 1. Flavivirus genus is highlighted in blue, Pestivirus is in green and Hepacivirus is in salmon. Flavivirus taxon was further divided according to host range: orange - insect-only, purple - NKV, yellow - mosquito-borne, red - tick-borne. Acronyms and names of viruses are defined in the “viral dataset” section.
Figure 5 Hierarchical clustering of Flaviviridae viruses and their hosts based on codon usage likeness. RSCU values were calculated for codons with degeneracy greater than one for every organism, generating a matrix of N×M dimensions, being N the number of species and M the number of degenerated codons. Hierarchical clustering of organisms was conducted based on Spearman's rho correlation coefficients of RSCU values. Color schema for clusters is the same used in Figure 1. Flavivirus genus is highlighted in blue, Pestivirus is in green and Hepacivirus is in salmon. Flavivirus taxon was further divided according to host range: orange - insect-only, purple - NKV, yellow - mosquito-borne, red - tick-borne. Acronyms and names of viruses are defined in the “viral dataset” section.CC BY · PubMed Central

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Research works printed but not linked: 2

  1. [16]Belshaw R de Oliveira T Markowitz S Rambaut A 2009 The RNA virus database. Nucleic Acids Res 37 D431 435 18948277 PMC2686580
  2. [86]Benson DA Karsch-Mizrachi I Lipman DJ Ostell J Sayers EW 2008 GenBank. Nucleic Acids Res PMC2686462 18940867

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Metadata

Authors
Lobo, F. P., Mota, B. E. F., Pena, S. D. J., Azevedo, V., Macedo, A. M., Tauch, A., Machado, C. R., & Franco, G. R.
Affiliations
  • Universidade Federal de Minas Gerais (BR)
  • Bielefeld University (DE)
Corresponding author
Lobo, Francisco P.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2009-07-20
Volume
4
Issue
7
Pages
e6282
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0006282
PMC
PMC2707012
OpenAlex
W1978006472
Cited by
191
References
98
Citations by year
2026: 7 · 2025: 8 · 2024: 18 · 2023: 12 · 2022: 5 · 2021: 17 · 2020: 12 · 2019: 9 · 2018: 10 · 2017: 19 · 2016: 10 · 2015: 14 · 2014: 16 · 2013: 19 · 2012: 6
FWCI
2.02
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
  • Publikationen an der Universität Bielefeld (Universität Bielefeld) (submittedVersion)
Funders
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
host-virus coevolution, Flaviviridae, codon usage bias, host-virus interaction, Hepacivirus, flavivirus, mosquito hosts, vertebrate hosts, DNA methylation
MeSH terms
Animals, Base Sequence, Codon, Disease Vectors, Biological Evolution, Phylogeny, Flaviviridae, Host-Pathogen Interactions

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