Virus evolution : the emergence of new ideas (and re-emergence of old ones)

Reputed intractable, the question of the origin of viruses has long been neglected. In the modern literature 'Virus evolution' has come to refer to study more akin to population genetics, such as the world-wide scrutiny on new polymorphisms appearing daily in the H5N1 avian flu virus [1], than to the fundamental interrogation: where do viruses come from? This situation is now rapidly changing, due to the coincidence of bold new ideas (and sometimes the revival of old ones), the unexpected features exhibited by recently isolated spectacular viruses [2] (see at URL: www.giantvirus.org), as well as the steady increase of genomic sequences for 'regular' viruses and cellular organisms enhancing the power of comparative genomics [3]. After being considered non-living and relegated in the wings by a majority of biologists, viruses are now pushed back on the center stage: they might have been at the origin of DNA, of the eukaryotic cell, and even of today's partition of biological organisms into 3 domains of life: bacteria, archaea and eukarya. Here, I quickly survey some of the recent discoveries and the new evolutionary thoughts they have prompted, before adding to the confusion with one interrogation of my own: what if we totally missed the true nature of (at least some) viruses?Comment: submitte

Giant viruses in the oceans: the 4(th )Algal Virus Workshop

Giant double-stranded DNA viruses (such as record breaking Acanthamoeba polyphaga Mimivirus), with particle sizes of 0.2 to 0.6 μm, genomes of 300 kbp to 1.200 kbp, and commensurate complex gene contents, constitute an evolutionary mystery. They challenge the common vision of viruses, traditionally seen as highly streamlined genomes optimally fitted to the smallest possible -filterable- package. Such giant viruses are now discovered in increasing numbers through the systematic sampling of ocean waters as well as freshwater aquatic environments, where they play a significant role in controlling phyto- and bacterio- plankton populations. The 4(th )algal virus workshop showed that the study of these ecologically important viruses is now massively entering the genomic era, promising a better understanding of their diversity and, hopefully, some insights on their origin and the evolutionary forces that shaped their genomes

Mimivirus Relatives in the Sargasso Sea

The discovery and genome analysis of Acanthamoeba polyphaga Mimivirus, the largest known DNA virus, challenged much of the accepted dogma regarding viruses. Its particle size (>400 nm), genome length (1.2 million bp) and huge gene repertoire (911 protein coding genes) all contribute to blur the established boundaries between viruses and the smallest parasitic cellular organisms. Phylogenetic analyses also suggested that the Mimivirus lineage could have emerged prior to the individualization of cellular organisms from the three established domains, triggering a debate that can only be resolved by generating and analyzing more data. The next step is then to seek some evidence that Mimivirus is not the only representative of its kind and determine where to look for new Mimiviridae. An exhaustive similarity search of all Mimivirus predicted proteins against all publicly available sequences identified many of their closest homologues among the Sargasso Sea environmental sequences. Subsequent phylogenetic analyses suggested that unknown large viruses evolutionarily closer to Mimivirus than to any presently characterized species exist in abundance in the Sargasso Sea. Their isolation and genome sequencing could prove invaluable in understanding the origin and diversity of large DNA viruses, and shed some light on the role they eventually played in the emergence of eukaryotes.Comment: see also http://www.giantvirus.or

Metagrowth: a new resource for the building of metabolic hypotheses in microbiology

Metagrowth is a new type of knowledge base developed to guide the experimental studies of culture conditions of obligate parasitic bacteria. We have gathered biological evidences giving possible clues to the development of the axenic (i.e. ‘cell-free’) growth of obligate parasites from various sources including published literature, genomic sequence information, metabolic databases and transporter databases. The database entries are composed of those evidences and specific hypotheses derived from them. Currently, 200 entries are available for Rickettsia prowazekii, Rickettsia conorii, Tropheryma whipplei, Treponema pallidum, Mycobacterium tuberculosis and Coxiella burnetii. The web interface of Metagrowth helps users to design new axenic culture media eventually suitable for those bacteria. Metagrowth is accessible at http://igs-server.cnrs-mrs.fr/axenic/

Mimivirus reveals Mre11/Rad50 fusion proteins with a sporadic distribution in eukaryotes, bacteria, viruses and plasmids

<p>Abstract</p> <p>Background</p> <p>The Mre11/Rad50 complex and the homologous SbcD/SbcC complex in bacteria play crucial roles in the metabolism of DNA double-strand breaks, including DNA repair, genome replication, homologous recombination and non-homologous end-joining in cellular life forms and viruses. Here we investigated the amino acid sequence of the Mimivirus R555 gene product, originally annotated as a Rad50 homolog, and later shown to have close homologs in marine microbial metagenomes.</p> <p>Results</p> <p>Our bioinformatics analysis revealed that R555 protein sequence is constituted from the fusion of an N-terminal Mre11-like domain with a C-terminal Rad50-like domain. A systematic database search revealed twelve additional cases of Mre11/Rad50 (or SbcD/SbcC) fusions in a wide variety of unrelated organisms including unicellular and multicellular eukaryotes, the megaplasmid of a bacterium associated to deep-sea hydrothermal vents (<it>Deferribacter desulfuricans</it>) and the plasmid of <it>Clostridium kluyveri</it>. We also showed that R555 homologs are abundant in the metagenomes from different aquatic environments and that they most likely belong to aquatic viruses. The observed phyletic distribution of these fusion proteins suggests their recurrent creation and lateral gene transfers across organisms.</p> <p>Conclusions</p> <p>The existence of the fused version of protein sequences is consistent with known functional interactions between Mre11 and Rad50, and the gene fusion probably enhanced the opportunity for lateral transfer. The abundance of the Mre11/Rad50 fusion genes in viral metagenomes and their sporadic phyletic distribution in cellular organisms suggest that viruses, plasmids and transposons played a crucial role in the formation of the fusion proteins and their propagation into cellular genomes.</p

Horizontal gene transfer and nucleotide compositional anomaly in large DNA viruses

<p>Abstract</p> <p>Background</p> <p>DNA viruses have a wide range of genome sizes (5 kb up to 1.2 Mb, compared to 0.16 Mb to 1.5 Mb for obligate parasitic bacteria) that do not correlate with their virulence or the taxonomic distribution of their hosts. The reasons for such large variation are unclear. According to the traditional view of viruses as gifted "gene pickpockets", large viral genome sizes could originate from numerous gene acquisitions from their hosts. We investigated this hypothesis by studying 67 large DNA viruses with genome sizes larger than 150 kb, including the recently characterized giant mimivirus. Given that horizontally transferred DNA often have anomalous nucleotide compositions differing from the rest of the genome, we conducted a detailed analysis of the inter- and intra-genome compositional properties of these viruses. We then interpreted their compositional heterogeneity in terms of possible causes, including strand asymmetry, gene function/expression, and horizontal transfer.</p> <p>Results</p> <p>We first show that the global nucleotide composition and nucleotide word usage of viral genomes are species-specific and distinct from those of their hosts. Next, we identified compositionally anomalous (cA) genes in viral genomes, using a method based on Bayesian inference. The proportion of cA genes is highly variable across viruses and does not exhibit a significant correlation with genome size. The vast majority of the cA genes were of unknown function, lacking homologs in the databases. For genes with known homologs, we found a substantial enrichment of cA genes in specific functional classes for some of the viruses. No significant association was found between cA genes and compositional strand asymmetry. A possible exogenous origin for a small fraction of the cA genes could be confirmed by phylogenetic reconstruction.</p> <p>Conclusion</p> <p>At odds with the traditional dogma, our results argue against frequent genetic transfers to large DNA viruses from their modern hosts. The large genome sizes of these viruses are not simply explained by an increased propensity to acquire foreign genes. This study also confirms that the anomalous nucleotide compositions of the cA genes is sometimes linked to particular biological functions or expression patterns, possibly leading to an overestimation of recent horizontal gene transfers.</p