Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses

Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an...

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Published in:PloS one Vol. 11; no. 4; p. e0154376
Main Authors: Kumar, Naveen, Bera, Bidhan Chandra, Greenbaum, Benjamin D., Bhatia, Sandeep, Sood, Richa, Selvaraj, Pavulraj, Anand, Taruna, Tripathi, Bhupendra Nath, Virmani, Nitin
Format: Journal Article
Language:English
Published: United States Public Library of Science 27.04.2016
Public Library of Science (PLoS)
Subjects:
Adaptability
Adaptation
Adaptation, Physiological - genetics
Analysis
Animals
Avian influenza viruses
Bias
Biological Evolution
Biology and Life Sciences
Codon
Codon bias
Codons
Data processing
Fitness
Gene amplification
Gene Expression Regulation, Viral
Genetic Code
Genome, Viral
Genomes
Health aspects
Horse Diseases - virology
Horses
Host-Pathogen Interactions
Influenza
Influenza A Virus, H3N8 Subtype - genetics
Influenza A Virus, H3N8 Subtype - metabolism
Influenza A Virus, H7N7 Subtype - genetics
Influenza A Virus, H7N7 Subtype - metabolism
Interferon
Machinery
Machinery and equipment
Medicine and Health Sciences
Models, Statistical
Mutation
Mutation Rate
Natural selection
Orthomyxoviridae
Orthomyxoviridae Infections - veterinary
Orthomyxoviridae Infections - virology
Outbreaks
Pandemics
Pressure
Reproductive fitness
RNA, Transfer - genetics
RNA, Transfer - metabolism
Species Specificity
Statistical methods
Transfer RNA
tRNA
Vaccines
Virus Replication
Viruses
New York
United States > US
India
ISSN:1932-6203, 1932-6203
Online Access:Get full text
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Abstract Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an absolute dependence on the host cellular machinery for their replication. In the present study, we analyzed genome-wide codon usage patterns in 92 EIV strains, including both H3N8 and H7N7 subtypes by computing several codon usage indices and applying multivariate statistical methods. Relative synonymous codon usage (RSCU) analysis disclosed bias of preferred synonymous codons towards A/U-ended codons. The overall codon usage bias in EIVs was slightly lower, and mainly affected by the nucleotide compositional constraints as inferred from the RSCU and effective number of codon (ENc) analysis. Our data suggested that codon usage pattern in EIVs is governed by the interplay of mutation pressure, natural selection from its hosts and undefined factors. The H7N7 subtype was found less fit to its host (horse) in comparison to H3N8, by possessing higher codon bias, lower mutation pressure and much less adaptation to tRNA pool of equine cells. To the best of our knowledge, this is the first report describing the codon usage analysis of the complete genomes of EIVs. The outcome of our study is likely to enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.
AbstractList Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an absolute dependence on the host cellular machinery for their replication. In the present study, we analyzed genome-wide codon usage patterns in 92 EIV strains, including both H3N8 and H7N7 subtypes by computing several codon usage indices and applying multivariate statistical methods. Relative synonymous codon usage (RSCU) analysis disclosed bias of preferred synonymous codons towards A/U-ended codons. The overall codon usage bias in EIVs was slightly lower, and mainly affected by the nucleotide compositional constraints as inferred from the RSCU and effective number of codon (ENc) analysis. Our data suggested that codon usage pattern in EIVs is governed by the interplay of mutation pressure, natural selection from its hosts and undefined factors. The H7N7 subtype was found less fit to its host (horse) in comparison to H3N8, by possessing higher codon bias, lower mutation pressure and much less adaptation to tRNA pool of equine cells. To the best of our knowledge, this is the first report describing the codon usage analysis of the complete genomes of EIVs. The outcome of our study is likely to enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.
Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an absolute dependence on the host cellular machinery for their replication. In the present study, we analyzed genome-wide codon usage patterns in 92 EIV strains, including both H3N8 and H7N7 subtypes by computing several codon usage indices and applying multivariate statistical methods. Relative synonymous codon usage (RSCU) analysis disclosed bias of preferred synonymous codons towards A/U-ended codons. The overall codon usage bias in EIVs was slightly lower, and mainly affected by the nucleotide compositional constraints as inferred from the RSCU and effective number of codon (ENc) analysis. Our data suggested that codon usage pattern in EIVs is governed by the interplay of mutation pressure, natural selection from its hosts and undefined factors. The H7N7 subtype was found less fit to its host (horse) in comparison to H3N8, by possessing higher codon bias, lower mutation pressure and much less adaptation to tRNA pool of equine cells. To the best of our knowledge, this is the first report describing the codon usage analysis of the complete genomes of EIVs. The outcome of our study is likely to enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant outbreaks worldwide. Adaptability of influenza viruses to a particular host is significantly influenced by their codon usage preference, due to an absolute dependence on the host cellular machinery for their replication. In the present study, we analyzed genome-wide codon usage patterns in 92 EIV strains, including both H3N8 and H7N7 subtypes by computing several codon usage indices and applying multivariate statistical methods. Relative synonymous codon usage (RSCU) analysis disclosed bias of preferred synonymous codons towards A/U-ended codons. The overall codon usage bias in EIVs was slightly lower, and mainly affected by the nucleotide compositional constraints as inferred from the RSCU and effective number of codon (ENc) analysis. Our data suggested that codon usage pattern in EIVs is governed by the interplay of mutation pressure, natural selection from its hosts and undefined factors. The H7N7 subtype was found less fit to its host (horse) in comparison to H3N8, by possessing higher codon bias, lower mutation pressure and much less adaptation to tRNA pool of equine cells. To the best of our knowledge, this is the first report describing the codon usage analysis of the complete genomes of EIVs. The outcome of our study is likely to enhance our understanding of factors involved in viral adaptation, evolution, and fitness towards their hosts.
Audience Academic
Author Greenbaum, Benjamin D.
Virmani, Nitin
Sood, Richa
Selvaraj, Pavulraj
Bhatia, Sandeep
Kumar, Naveen
Anand, Taruna
Bera, Bidhan Chandra
Tripathi, Bhupendra Nath
AuthorAffiliation 3 Tisch Cancer Institute, Departments of Medicine, Hematology and Medical Pathology, and Pathology, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America
1 Immunology Lab, National Institute of High Security Animal Diseases (NIHSAD), Bhopal, Madhya Pradesh, India
Centers for Disease Control and Prevention, UNITED STATES
2 Biotechnology Lab, Veterinary Type Culture Collection, National Research Center on Equines (NRCE), Hisar, Haryana, India
4 Equine Pathology Lab, National Research Center on Equines (NRCE), Hisar, Haryana, India
AuthorAffiliation_xml – name: 3 Tisch Cancer Institute, Departments of Medicine, Hematology and Medical Pathology, and Pathology, Icahn School of Medicine at Mount Sinai, New York, New York, United States of America
– name: 2 Biotechnology Lab, Veterinary Type Culture Collection, National Research Center on Equines (NRCE), Hisar, Haryana, India
– name: 1 Immunology Lab, National Institute of High Security Animal Diseases (NIHSAD), Bhopal, Madhya Pradesh, India
– name: 4 Equine Pathology Lab, National Research Center on Equines (NRCE), Hisar, Haryana, India
– name: Centers for Disease Control and Prevention, UNITED STATES
Author_xml – sequence: 1
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  surname: Kumar
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  fullname: Greenbaum, Benjamin D.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/27119730$$D View this record in MEDLINE/PubMed
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Conceived and designed the experiments: NV BCB NK. Performed the experiments: NV BDG NK. Analyzed the data: NK BDG BCB. Contributed reagents/materials/analysis tools: TA BNT BDG RS PS NK. Wrote the paper: NK NV BCB BDG SB.
Competing Interests: The authors have declared that no competing interests exist.
These authors also contributed equally to this work.
ORCID 0000-0001-5575-3307
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Snippet Equine influenza viruses (EIVs) of H3N8 subtype are culprits of severe acute respiratory infections in horses, and are still responsible for significant...
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SubjectTerms Adaptability
Adaptation
Adaptation, Physiological - genetics
Analysis
Animals
Avian influenza viruses
Bias
Biological Evolution
Biology and Life Sciences
Codon
Codon bias
Codons
Data processing
Fitness
Gene amplification
Gene Expression Regulation, Viral
Genetic Code
Genome, Viral
Genomes
Health aspects
Horse Diseases - virology
Horses
Host-Pathogen Interactions
Influenza
Influenza A Virus, H3N8 Subtype - genetics
Influenza A Virus, H3N8 Subtype - metabolism
Influenza A Virus, H7N7 Subtype - genetics
Influenza A Virus, H7N7 Subtype - metabolism
Interferon
Machinery
Machinery and equipment
Medicine and Health Sciences
Models, Statistical
Mutation
Mutation Rate
Natural selection
Orthomyxoviridae
Orthomyxoviridae Infections - veterinary
Orthomyxoviridae Infections - virology
Outbreaks
Pandemics
Pressure
Reproductive fitness
RNA, Transfer - genetics
RNA, Transfer - metabolism
Species Specificity
Statistical methods
Transfer RNA
tRNA
Vaccines
Virus Replication
Viruses
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Title Revelation of Influencing Factors in Overall Codon Usage Bias of Equine Influenza Viruses
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http://dx.doi.org/10.1371/journal.pone.0154376
Volume 11
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