Comparative analysis of avian poxvirus genomes, including a novel poxvirus from lesser flamingos ( Phoenicopterus minor ), highlights the lack of conservation of the central region

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Abstract

Background

Avian poxviruses are important pathogens of both wild and domestic birds. To date, seven isolates from subclades A and B and one from proposed subclade E, have had their genomes completely sequenced. The genomes of these isolates have been shown to exhibit typical poxvirus genome characteristics with conserved central regions and more variable terminal regions. Infection with avian poxviruses (APVs) has been reported in three species of captive flamingo, as well as a free-living, lesser flamingo at Kamfers dam, near Kimberley, South Africa. This study was undertaken to further characterise this virus which may have long term effects on this important and vulnerable, breeding population.

Results

Gene content and synteny as well as percentage identities between conserved orthologues was compared between Flamingopox virus (FGPV) and the other sequenced APV genomes. Dotplot comparisons revealed major differences in central regions that have been thought to be conserved. Further analysis revealed five regions of difference, of differing lengths, spread across the central, conserved regions of the various genomes. Although individual gene identities at the nucleotide level did not vary greatly, gene content and synteny between isolates/species at these identified regions were more divergent than expected.

Conclusion

Basic comparative genomics revealed the expected similarities in genome architecture but an in depth, comparative, analysis showed all avian poxvirus genomes to differ from other poxvirus genomes in fundamental and unexpected ways. The reasons for these large genomic rearrangements in regions of the genome that were thought to be relatively conserved are yet to be elucidated. Sequencing and analysis of further avian poxvirus genomes will help characterise this complex genus of poxviruses.

Electronic supplementary material

The online version of this article (10.1186/s12864-017-4315-0) contains supplementary material, which is available to authorized users.

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Most cited references 36

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Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses.

Nels C. Elde, Stephanie J. Child, Michael T. Eickbush … (2012)

In contrast to RNA viruses, double-stranded DNA viruses have low mutation rates yet must still adapt rapidly in response to changing host defenses. To determine mechanisms of adaptation, we subjected the model poxvirus vaccinia to serial propagation in human cells, where its antihost factor K3L is maladapted against the antiviral protein kinase R (PKR). Viruses rapidly acquired higher fitness via recurrent K3L gene amplifications, incurring up to 7%-10% increases in genome size. These transient gene expansions were necessary and sufficient to counteract human PKR and facilitated the gain of an adaptive amino acid substitution in K3L that also defeats PKR. Subsequent reductions in gene amplifications offset the costs associated with larger genome size while retaining adaptive substitutions. Our discovery of viral "gene-accordions" explains how poxviruses can rapidly adapt to defeat different host defenses despite low mutation rates and reveals how classical Red Queen conflicts can progress through unrecognized intermediates. Copyright © 2012 Elsevier Inc. All rights reserved.

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Poxvirus genomes: a phylogenetic analysis.

Kellie N Smith, Caroline Gubser, Paul Kellam … (2003)

The evolutionary relationships of 26 sequenced members of the poxvirus family have been investigated by comparing their genome organization and gene content and by using DNA and protein sequences for phylogenetic analyses. The central region of the genome of chordopoxviruses (ChPVs) is highly conserved in gene content and arrangement, except for some gene inversions in Fowlpox virus (FPV) and species-specific gene insertions in FPV and Molluscum contagiosum virus (MCV). In the central region 90 genes are conserved in all ChPVs, but no gene from near the termini is conserved throughout the subfamily. Inclusion of two entomopoxvirus (EnPV) sequences reduces the number of conserved genes to 49. The EnPVs are divergent from ChPVs and between themselves. Relationships between ChPV genera were evaluated by comparing the genome size, number of unique genes, gene arrangement and phylogenetic analyses of protein sequences. Overall, genus Avipoxvirus is the most divergent. The next most divergent ChPV genus is Molluscipoxvirus, whose sole member, MCV, infects only man. The Suipoxvirus, Capripoxvirus, Leporipoxvirus and Yatapoxvirus genera cluster together, with Suipoxvirus and Capripoxvirus sharing a common ancestor, and are distinct from the genus Orthopoxvirus (OPV). Within the OPV genus, Monkeypox virus, Ectromelia virus and Cowpox virus strain Brighton Red (BR) do not group closely with any other OPV, Variola virus and Camelpox virus form a subgroup, and Vaccinia virus is most closely related to CPV-GRI-90. This suggests that CPV-BR and GRI-90 should be separate species.

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Orthopoxvirus Genome Evolution: The Role of Gene Loss

Robert Hendrickson, Chunlin Wang, Eneida Hatcher … (2010)

Poxviruses are highly successful pathogens, known to infect a variety of hosts. The family Poxviridae includes Variola virus, the causative agent of smallpox, which has been eradicated as a public health threat but could potentially reemerge as a bioterrorist threat. The risk scenario includes other animal poxviruses and genetically engineered manipulations of poxviruses. Studies of orthologous gene sets have established the evolutionary relationships of members within the Poxviridae family. It is not clear, however, how variations between family members arose in the past, an important issue in understanding how these viruses may vary and possibly produce future threats. Using a newly developed poxvirus-specific tool, we predicted accurate gene sets for viruses with completely sequenced genomes in the genus Orthopoxvirus. Employing sensitive sequence comparison techniques together with comparison of syntenic gene maps, we established the relationships between all viral gene sets. These techniques allowed us to unambiguously identify the gene loss/gain events that have occurred over the course of orthopoxvirus evolution. It is clear that for all existing Orthopoxvirus species, no individual species has acquired protein-coding genes unique to that species. All existing species contain genes that are all present in members of the species Cowpox virus and that cowpox virus strains contain every gene present in any other orthopoxvirus strain. These results support a theory of reductive evolution in which the reduction in size of the core gene set of a putative ancestral virus played a critical role in speciation and confining any newly emerging virus species to a particular environmental (host or tissue) niche.

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Author and article information

Contributors

Olivia Carulei: ocarulei@gmail.com

Nicola Douglass: Niki.Douglass@uct.ac.za

Anna-Lise Williamson:

ORCID: http://orcid.org/0000-0002-5467-1200

Anna-Lise.Williamson@uct.ac.za

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 6 December 2017

Publication date PMC-release: 6 December 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 947

Affiliations

[1 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Division of Medical Virology, Department of Pathology, Faculty of Health Sciences, , University of Cape Town, ; Cape Town, South Africa

[2 ]ISNI 0000 0004 1937 1151, GRID grid.7836.a, Institute of Infectious Disease and Molecular Medicine, , University of Cape Town, ; Cape Town, South Africa

[3 ]ISNI 0000 0004 0630 4574, GRID grid.416657.7, National Health Laboratory Service, ; Cape Town, South Africa

Author information

Anna-Lise Williamson http://orcid.org/0000-0002-5467-1200

Article

Publisher ID: 4315

DOI: 10.1186/s12864-017-4315-0

PMC ID: 5718139

PubMed ID: 29207949

SO-VID: 95672b00-633d-4d13-b90a-de2c80cb2dd6

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 13 July 2017

Date accepted : 17 November 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: Clinical Infectious Diseases Research Initiative (CIDRI)

Award Recipient : Olivia Carulei

Funded by: National Research Foundation (South Africa)

Award ID: NA

Award Recipient : Anna-Lise Williamson

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: poxvirus,avipoxvirus,flamingopox,genome sequence

Data availability:

ScienceOpen disciplines: Genetics

Keywords: poxvirus, avipoxvirus, flamingopox, genome sequence

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Comparative analysis of avian poxvirus genomes, including a novel poxvirus from lesser flamingos ( Phoenicopterus minor), highlights the lack of conservation of the central region

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Arabidopsis genomics

Most cited references 36

Poxviruses deploy genomic accordions to adapt rapidly against host antiviral defenses.

Poxvirus genomes: a phylogenetic analysis.

Orthopoxvirus Genome Evolution: The Role of Gene Loss

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