Poxvirus protein evolution: Family wide assessment of possible horizontal gene transfer events

Abstract To investigate the evolutionary origins of proteins encoded by the Poxviridae family of viruses, we examined all poxvirus protein coding genes using a method of characterizing and visualizing the similarity between these proteins and taxonomic subsets of proteins in GenBank. Our analysis divides poxvirus proteins into categories based on their relative degree of similarity to two different taxonomic subsets of proteins such as all eukaryote vs. all virus (except poxvirus) proteins. As an example, this allows us to identify, based on high similarity to only eukaryote proteins, poxvirus proteins that may have been obtained by horizontal transfer from their hosts. Although this method alone does not definitively prove horizontal gene transfer, it allows us to provide an assessment of the possibility of horizontal gene transfer for every poxvirus protein. Potential candidates can then be individually studied in more detail during subsequent investigation. Results of our analysis demonstrate that in general, proteins encoded by members of the subfamily Chordopoxvirinae exhibit greater similarity to eukaryote proteins than to proteins of other virus families. In addition, our results reiterate the important role played by host gene capture in poxvirus evolution; highlight the functions of many genes poxviruses share with their hosts; and illustrate which host-like genes are present uniquely in poxviruses and which are also present in other virus families.

[1]  E. Koonin,et al.  Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world , 2008, Nucleic acids research.

[2]  P. Kellam,et al.  Poxvirus genomes: a phylogenetic analysis. , 2004, The Journal of general virology.

[3]  Henry V. Baker,et al.  Myxoma viral serpin, Serp‐1, inhibits human monocyte adhesion through regulation of actin‐binding protein filamin B , 2009, Journal of leukocyte biology.

[4]  G. McFadden,et al.  Host-related immunomodulators encoded by poxviruses and herpesviruses. , 2000, Current opinion in microbiology.

[5]  T. Luque,et al.  Insect-virus relationships: sifting by informatics. , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  E. Koonin,et al.  The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. , 1997, Virology.

[7]  Kirsten A. Bratke,et al.  Identification of multiple independent horizontal gene transfers into poxviruses using a comparative genomics approach , 2008, BMC Evolutionary Biology.

[8]  L. Koski,et al.  The Closest BLAST Hit Is Often Not the Nearest Neighbor , 2001, Journal of Molecular Evolution.

[9]  G. McFadden,et al.  Immunopathogenesis of poxvirus infections: forecasting the impending storm , 2007, Immunology and cell biology.

[10]  L. Katz,et al.  Lateral gene transfers and the evolution of eukaryotes: theories and data. , 2002, International journal of systematic and evolutionary microbiology.

[11]  S. Kaufmann,et al.  Modulation of T cell development and activation by novel members of the Schlafen (slfn) gene family harbouring an RNA helicase-like motif. , 2004, International immunology.

[12]  J. Drake,et al.  On the Mutation Rate of Herpes Simplex Virus Type 1 , 2005, Genetics.

[13]  Derrick J. Zwickl Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion , 2006 .

[14]  G. McFadden,et al.  The role of cell signaling in poxvirus tropism: the case of the M-T5 host range protein of myxoma virus. , 2008, Biochimica et biophysica acta.

[15]  B. Finlay,et al.  Anti-Immunology: Evasion of the Host Immune System by Bacterial and Viral Pathogens , 2006, Cell.

[16]  E. Koonin,et al.  Common Origin of Four Diverse Families of Large Eukaryotic DNA Viruses , 2001, Journal of Virology.

[17]  D. Botstein A THEORY OF MODULAR EVOLUTION FOR BACTERIOPHAGES * , 1980, Annals of the New York Academy of Sciences.

[18]  D. Rock,et al.  Genome of Horsepox Virus , 2006, Journal of Virology.

[19]  E. Koonin,et al.  Evolution of thymidine and thymidylate kinases: The possibility of independent capture of TK genes by different groups of viruses , 1992, Virus Genes.

[20]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[21]  S. Shchelkunov,et al.  The genomic sequence analysis of the left and right species-specific terminal region of a cowpox virus strain reveals unique sequences and a cluster of intact ORFs for immunomodulatory and host range proteins. , 1998, Virology.

[22]  J. H. Strauss,et al.  Virus Evolution , 2001, Cell.

[23]  J. Claverie,et al.  Horizontal gene transfer and nucleotide compositional anomaly in large DNA viruses , 2007, BMC Genomics.

[24]  A. Dishon,et al.  Cyprinid herpes virus‐3 (CyHV‐3) bears genes of genetically distant large DNA viruses , 2006, FEBS letters.

[25]  Kyong-Tai Kim,et al.  VRK1 phosphorylates CREB and mediates CCND1 expression , 2008, Journal of Cell Science.

[26]  J. Whisstock,et al.  The Serpins Are an Expanding Superfamily of Structurally Similar but Functionally Diverse Proteins , 2001, The Journal of Biological Chemistry.

[27]  E. Holmes,et al.  Rates of evolutionary change in viruses: patterns and determinants , 2008, Nature Reviews Genetics.

[28]  C. Upton,et al.  Host-derived pathogenicity islands in poxviruses , 2005, Virology Journal.

[29]  A. Hughes,et al.  Poxvirus genome evolution by gene gain and loss. , 2005, Molecular phylogenetics and evolution.

[30]  A. Hughes Origin and Evolution of Viral Interleukin-10 and Other DNA Virus Genes with Vertebrate Homologues , 2002, Journal of Molecular Evolution.

[31]  Paula Traktman,et al.  In a nutshell: structure and assembly of the vaccinia virion. , 2006, Advances in virus research.

[32]  Yu Li,et al.  On the origin of smallpox: Correlating variola phylogenics with historical smallpox records , 2007, Proceedings of the National Academy of Sciences.

[33]  E. Holmes,et al.  The evolution of large DNA viruses: combining genomic information of viruses and their hosts. , 2004, Trends in microbiology.

[34]  Chris Upton,et al.  Poxvirus Bioinformatics Resource Center: a comprehensive Poxviridae informational and analytical resource , 2004, Nucleic Acids Res..

[35]  Brandon S. Gaut,et al.  Extensive gene gain associated with adaptive evolution of poxviruses , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Aloy,et al.  Ribonucleotide Reductases: Divergent Evolution of an Ancient Enzyme , 2002, Journal of Molecular Evolution.

[37]  D. Rock,et al.  The Genome of Fowlpox Virus , 2000, Journal of Virology.

[38]  C Upton,et al.  Poxviruses: past, present and future. , 2006, Virus research.

[39]  G. McFadden,et al.  Poxviruses and immune evasion. , 2003, Annual review of immunology.

[40]  Eugene V Koonin,et al.  Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. , 2006, Virus research.

[41]  P. Reichard,et al.  Ribonucleotide reductases. , 1998, Annual review of biochemistry.

[42]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[43]  A. Gould,et al.  Field and vaccine strains of fowlpox virus carry integrated sequences from the avian retrovirus, reticuloendotheliosis virus. , 1997, Virology.

[44]  Jacques Ravel,et al.  Visualization of comparative genomic analyses by BLAST score ratio , 2005, BMC Bioinformatics.

[45]  M. Skinner,et al.  Fowlpox Virus Encodes Nonessential Homologs of Cellular Alpha-SNAP, PC-1, and an Orphan Human Homolog of a Secreted Nematode Protein , 1998, Journal of Virology.

[46]  R. J. Clem,et al.  Identification and functional characterization of AMVp33, a novel homolog of the baculovirus caspase inhibitor p35 found in Amsacta moorei entomopoxvirus. , 2007, Virology.

[47]  Rachel L. Roper,et al.  Poxvirus Orthologous Clusters: toward Defining the Minimum Essential Poxvirus Genome , 2003, Journal of Virology.

[48]  P. Formenty,et al.  A tale of two clades: monkeypox viruses. , 2005, The Journal of general virology.

[49]  K. Xing,et al.  Genome-Based Phylogeny of Poxvirus , 2006, Intervirology.

[50]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..