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Open Access Research article

Phylogenetic evidence for extensive lateral acquisition of cellular genes by Nucleocytoplasmic large DNA viruses

Jonathan Filée*, Noëlle Pouget and Mick Chandler

Author Affiliations

Laboratoire de Microbiologie et Génétique Moléculaires, C.N.R.S, Campus Toulouse III, 118 Route de Narbonne, F-31062 Toulouse Cedex, France

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BMC Evolutionary Biology 2008, 8:320  doi:10.1186/1471-2148-8-320

Published: 26 November 2008

Abstract

Background

Nucleo-Cytoplasmic Large DNA viruses (NCLDV), a diverse group that infects a wide range of eukaryotic hosts, exhibit a large heterogeneity in genome size (between 100 kb and 1.2 Mb) but have been suggested to form a monophyletic group on the basis of a small subset of approximately 30 conserved genes. NCLDV were proposed to have evolved by simplification from cellular organism although some of the giant NCLDV have clearly grown by gene accretion from a bacterial origin.

Results

We demonstrate here that many NCLDV lineages appear to have undergone frequent gene exchange in two different ways. Viruses which infect protists directly (Mimivirus) or algae which exist as intracellular protists symbionts (Phycodnaviruses) acquire genes from a bacterial source. Metazoan viruses such as the Poxviruses show a predominant acquisition of host genes. In both cases, the laterally acquired genes show a strong tendency to be positioned at the tip of the genome. Surprisingly, several core genes believed to be ancestral in the family appear to have undergone lateral gene transfers, suggesting that the NCLDV ancestor might have had a smaller genome than previously believed. Moreover, our data show that the larger the genome, the higher is the number of laterally acquired genes. This pattern is incompatible with a genome reduction from a cellular ancestor.

Conclusion

We propose that the NCLDV viruses have evolved by significant growth of a simple DNA virus by gene acquisition from cellular sources.