Abstract
BackgroundNucleo-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.ResultsWe 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.ConclusionWe propose that the NCLDV viruses have evolved by significant growth of a simple DNA virus by gene acquisition from cellular sources.
Highlights
Nucleo-Cytoplasmic Large DNA viruses (NCLDV), a diverse group that infects a wide range of eukaryotic hosts, exhibit a large heterogeneity in genome size but have been suggested to form a monophyletic group on the basis of a small subset of approximately 30 conserved genes
Bacterial-like genes are less frequent in Phycodnaviruses of free living algae We suggested that their eukaryotic hosts, which graze on bacteria, could provide the "ecological" niche for viral access to bacterial gene pools
This analysis probably over-estimated the level of inter-virus gene transfers because some of them are probably the results of independent genes acquisitions from the hosts. These results show that most, if not all, of the host derived genes identified in this study do not have a viral origin and constitute bona fide evidences of host-to-virus gene transfers. In this and the previous study [27], we have shown that the large diversity of the genomic repertoire of the different lineages of NCLDV can be explained principally by the accretion of a sizeable collection of cellular genes derived from their host and/or from bacteria
Summary
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. DNA viruses are ubiquitous components of the biosphere and their number exceeds that of cells by at least an order of magnitude [1] This abundance is accompanied by an extraordinary diversity in genome size, composition and organisation [2] and viruses have been divided into many different classes based on these criteria. - The "virus first" hypothesis proposes that viruses are descendants of primordial genetic elements that were components of the primitive soup [5]. These hypotheses have been extensively discussed in the light of recent advances in comparative genomics (see for example [6] and [7] and references therein). Mimivirus has a genome of 1.2 Mb, significantly larger than that of several bacteria [9]
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