Eukaryotic large nucleo-cytoplasmic DNA viruses: Clusters of orthologous genes and reconstruction of viral genome evolution

Natalya Yutin,Yuri I Wolf,Didier Raoult,Eugene V Koonin

doi:10.1186/1743-422x-6-223

Abstract

BackgroundThe Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) comprise an apparently monophyletic class of viruses that infect a broad variety of eukaryotic hosts. Recent progress in isolation of new viruses and genome sequencing resulted in a substantial expansion of the NCLDV diversity, resulting in additional opportunities for comparative genomic analysis, and a demand for a comprehensive classification of viral genes.ResultsA comprehensive comparison of the protein sequences encoded in the genomes of 45 NCLDV belonging to 6 families was performed in order to delineate cluster of orthologous viral genes. Using previously developed computational methods for orthology identification, 1445 Nucleo-Cytoplasmic Virus Orthologous Groups (NCVOGs) were identified of which 177 are represented in more than one NCLDV family. The NCVOGs were manually curated and annotated and can be used as a computational platform for functional annotation and evolutionary analysis of new NCLDV genomes. A maximum-likelihood reconstruction of the NCLDV evolution yielded a set of 47 conserved genes that were probably present in the genome of the common ancestor of this class of eukaryotic viruses. This reconstructed ancestral gene set is robust to the parameters of the reconstruction procedure and so is likely to accurately reflect the gene core of the ancestral NCLDV, indicating that this virus encoded a complex machinery of replication, expression and morphogenesis that made it relatively independent from host cell functions.ConclusionsThe NCVOGs are a flexible and expandable platform for genome analysis and functional annotation of newly characterized NCLDV. Evolutionary reconstructions employing NCVOGs point to complex ancestral viruses.

Highlights

Viruses span approximately 3 orders of magnitude (~103 to ~106 nucleotides) in genome size and show tremendous diversity of virion architecture, size and complexity [1,2,3]
Clusters of orthologous genes for the Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) (NCVOGs) In this works, we analyzed the annotated proteins encoded in 45 NCLDV proteomes from 6 viral families (Tables 1 and Additional file 1)
DFiigsturribeu2tion of the number of NCLDV species represented in Nucleo-Cytoplasmic Virus Orthologous Groups (NCVOGs) Distribution of the number of NCLDV species represented in NCVOGs

Summary

Introduction

Viruses span approximately 3 orders of magnitude (~103 to ~106 nucleotides) in genome size and show tremendous diversity of virion architecture, size and complexity [1,2,3]. One of the most expansive, apparently monophyletic divisions of viruses consists of at least 6 families of eukaryotic viruses with large DNA genomes including Poxviridae, an expansive viral family that includes major pathogens of humans and other mammals These viruses infect animals and diverse unicellular eukaryotes, and replicate either exclusively in the cytoplasm of the host cells, or possess both cytoplasmic and nuclear stages in their life cycle (Table 1). These viral families have been collectively designated Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) [5,6]. Recent progress in isolation of new viruses and genome sequencing resulted in a substantial expansion of the NCLDV diversity, resulting in additional opportunities for comparative genomic analysis, and a demand for a comprehensive classification of viral genes

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