Evolution of Genome Size and Complexity in the Rhabdoviridae

Peter J. Walker, Cadhla Firth, Steven Widen, Kim R. Blasdell, Hilda Guzman, Thomas Wood, Prasad N. Paradkar, Edward C. Holmes, Robert B. Tesh, Nikos Vasilakis

Research output: Contribution to journalArticle

71 Citations (Scopus)

Abstract

RNA viruses exhibit substantial structural, ecological and genomic diversity. However, genome size in RNA viruses is likely limited by a high mutation rate, resulting in the evolution of various mechanisms to increase complexity while minimising genome expansion. Here we conduct a large-scale analysis of the genome sequences of 99 animal rhabdoviruses, including 45 genomes which we determined de novo, to identify patterns of genome expansion and the evolution of genome complexity. All but seven of the rhabdoviruses clustered into 17 well-supported monophyletic groups, of which eight corresponded to established genera, seven were assigned as new genera, and two were taxonomically ambiguous. We show that the acquisition and loss of new genes appears to have been a central theme of rhabdovirus evolution, and has been associated with the appearance of alternative, overlapping and consecutive ORFs within the major structural protein genes, and the insertion and loss of additional ORFs in each gene junction in a clade-specific manner. Changes in the lengths of gene junctions accounted for as much as 48.5% of the variation in genome size from the smallest to the largest genome, and the frequency with which new ORFs were observed increased in the 3’ to 5’ direction along the genome. We also identify several new families of accessory genes encoded in these regions, and show that non-canonical expression strategies involving TURBS-like termination-reinitiation, ribosomal frame-shifts and leaky ribosomal scanning appear to be common. We conclude that rhabdoviruses have an unusual capacity for genomic plasticity that may be linked to their discontinuous transcription strategy from the negative-sense single-stranded RNA genome, and propose a model that accounts for the regular occurrence of genome expansion and contraction throughout the evolution of the Rhabdoviridae.

Original languageEnglish (US)
Article numbere1004664
JournalPLoS Pathogens
Volume11
Issue number2
DOIs
StatePublished - 2015

Fingerprint

Rhabdoviridae
Genome Size
Genome
Open Reading Frames
RNA Viruses
Genes
Ribosomal Frameshifting
Insertional Mutagenesis
Mutation Rate
Sequence Analysis
RNA

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

Evolution of Genome Size and Complexity in the Rhabdoviridae. / Walker, Peter J.; Firth, Cadhla; Widen, Steven; Blasdell, Kim R.; Guzman, Hilda; Wood, Thomas; Paradkar, Prasad N.; Holmes, Edward C.; Tesh, Robert B.; Vasilakis, Nikos.

In: PLoS Pathogens, Vol. 11, No. 2, e1004664, 2015.

Research output: Contribution to journalArticle

Walker, PJ, Firth, C, Widen, S, Blasdell, KR, Guzman, H, Wood, T, Paradkar, PN, Holmes, EC, Tesh, RB & Vasilakis, N 2015, 'Evolution of Genome Size and Complexity in the Rhabdoviridae', PLoS Pathogens, vol. 11, no. 2, e1004664. https://doi.org/10.1371/journal.ppat.1004664
Walker, Peter J. ; Firth, Cadhla ; Widen, Steven ; Blasdell, Kim R. ; Guzman, Hilda ; Wood, Thomas ; Paradkar, Prasad N. ; Holmes, Edward C. ; Tesh, Robert B. ; Vasilakis, Nikos. / Evolution of Genome Size and Complexity in the Rhabdoviridae. In: PLoS Pathogens. 2015 ; Vol. 11, No. 2.
@article{915e3477186444db87af2fb4349543ce,
title = "Evolution of Genome Size and Complexity in the Rhabdoviridae",
abstract = "RNA viruses exhibit substantial structural, ecological and genomic diversity. However, genome size in RNA viruses is likely limited by a high mutation rate, resulting in the evolution of various mechanisms to increase complexity while minimising genome expansion. Here we conduct a large-scale analysis of the genome sequences of 99 animal rhabdoviruses, including 45 genomes which we determined de novo, to identify patterns of genome expansion and the evolution of genome complexity. All but seven of the rhabdoviruses clustered into 17 well-supported monophyletic groups, of which eight corresponded to established genera, seven were assigned as new genera, and two were taxonomically ambiguous. We show that the acquisition and loss of new genes appears to have been a central theme of rhabdovirus evolution, and has been associated with the appearance of alternative, overlapping and consecutive ORFs within the major structural protein genes, and the insertion and loss of additional ORFs in each gene junction in a clade-specific manner. Changes in the lengths of gene junctions accounted for as much as 48.5{\%} of the variation in genome size from the smallest to the largest genome, and the frequency with which new ORFs were observed increased in the 3’ to 5’ direction along the genome. We also identify several new families of accessory genes encoded in these regions, and show that non-canonical expression strategies involving TURBS-like termination-reinitiation, ribosomal frame-shifts and leaky ribosomal scanning appear to be common. We conclude that rhabdoviruses have an unusual capacity for genomic plasticity that may be linked to their discontinuous transcription strategy from the negative-sense single-stranded RNA genome, and propose a model that accounts for the regular occurrence of genome expansion and contraction throughout the evolution of the Rhabdoviridae.",
author = "Walker, {Peter J.} and Cadhla Firth and Steven Widen and Blasdell, {Kim R.} and Hilda Guzman and Thomas Wood and Paradkar, {Prasad N.} and Holmes, {Edward C.} and Tesh, {Robert B.} and Nikos Vasilakis",
year = "2015",
doi = "10.1371/journal.ppat.1004664",
language = "English (US)",
volume = "11",
journal = "PLoS Pathogens",
issn = "1553-7366",
publisher = "Public Library of Science",
number = "2",

}

TY - JOUR

T1 - Evolution of Genome Size and Complexity in the Rhabdoviridae

AU - Walker, Peter J.

AU - Firth, Cadhla

AU - Widen, Steven

AU - Blasdell, Kim R.

AU - Guzman, Hilda

AU - Wood, Thomas

AU - Paradkar, Prasad N.

AU - Holmes, Edward C.

AU - Tesh, Robert B.

AU - Vasilakis, Nikos

PY - 2015

Y1 - 2015

N2 - RNA viruses exhibit substantial structural, ecological and genomic diversity. However, genome size in RNA viruses is likely limited by a high mutation rate, resulting in the evolution of various mechanisms to increase complexity while minimising genome expansion. Here we conduct a large-scale analysis of the genome sequences of 99 animal rhabdoviruses, including 45 genomes which we determined de novo, to identify patterns of genome expansion and the evolution of genome complexity. All but seven of the rhabdoviruses clustered into 17 well-supported monophyletic groups, of which eight corresponded to established genera, seven were assigned as new genera, and two were taxonomically ambiguous. We show that the acquisition and loss of new genes appears to have been a central theme of rhabdovirus evolution, and has been associated with the appearance of alternative, overlapping and consecutive ORFs within the major structural protein genes, and the insertion and loss of additional ORFs in each gene junction in a clade-specific manner. Changes in the lengths of gene junctions accounted for as much as 48.5% of the variation in genome size from the smallest to the largest genome, and the frequency with which new ORFs were observed increased in the 3’ to 5’ direction along the genome. We also identify several new families of accessory genes encoded in these regions, and show that non-canonical expression strategies involving TURBS-like termination-reinitiation, ribosomal frame-shifts and leaky ribosomal scanning appear to be common. We conclude that rhabdoviruses have an unusual capacity for genomic plasticity that may be linked to their discontinuous transcription strategy from the negative-sense single-stranded RNA genome, and propose a model that accounts for the regular occurrence of genome expansion and contraction throughout the evolution of the Rhabdoviridae.

AB - RNA viruses exhibit substantial structural, ecological and genomic diversity. However, genome size in RNA viruses is likely limited by a high mutation rate, resulting in the evolution of various mechanisms to increase complexity while minimising genome expansion. Here we conduct a large-scale analysis of the genome sequences of 99 animal rhabdoviruses, including 45 genomes which we determined de novo, to identify patterns of genome expansion and the evolution of genome complexity. All but seven of the rhabdoviruses clustered into 17 well-supported monophyletic groups, of which eight corresponded to established genera, seven were assigned as new genera, and two were taxonomically ambiguous. We show that the acquisition and loss of new genes appears to have been a central theme of rhabdovirus evolution, and has been associated with the appearance of alternative, overlapping and consecutive ORFs within the major structural protein genes, and the insertion and loss of additional ORFs in each gene junction in a clade-specific manner. Changes in the lengths of gene junctions accounted for as much as 48.5% of the variation in genome size from the smallest to the largest genome, and the frequency with which new ORFs were observed increased in the 3’ to 5’ direction along the genome. We also identify several new families of accessory genes encoded in these regions, and show that non-canonical expression strategies involving TURBS-like termination-reinitiation, ribosomal frame-shifts and leaky ribosomal scanning appear to be common. We conclude that rhabdoviruses have an unusual capacity for genomic plasticity that may be linked to their discontinuous transcription strategy from the negative-sense single-stranded RNA genome, and propose a model that accounts for the regular occurrence of genome expansion and contraction throughout the evolution of the Rhabdoviridae.

UR - http://www.scopus.com/inward/record.url?scp=84924351871&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84924351871&partnerID=8YFLogxK

U2 - 10.1371/journal.ppat.1004664

DO - 10.1371/journal.ppat.1004664

M3 - Article

C2 - 25679389

AN - SCOPUS:84924351871

VL - 11

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 2

M1 - e1004664

ER -