Evidence for extensive lateral acquisition of cellular genes by nucleocytoplasmic large DNA viruses

Jonathan Filée1; Michael Chandler2
1LEGS / CNRS, Avenue de la Terrasse, 91198 Gif sur Yvette CEDEX, France
2LMGM / CNRS, 118 Route de Narbonne, 31062 Toulouse CEDEX, France

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 100kb and 1.2Mb) but have been suggested to form a monophyletic group on the basis of a small subset of approximately 30 conserved genes. We demonstrate 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 protist 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. We propose that the NCLDV viruses have evolved by significant growth of a simple DNA virus by gene acquisition from cellular sources.

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