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

Evolutionary Dynamics of Giant Viruses and their Virophages

Giant viruses contain large genomes, encode many proteins atypical for viruses, replicate in large viral factories, and tend to infect protists. The giant virus replication factories can in turn be infected by so called virophages, which are smaller viruses that negatively impact giant virus replication. An example are Mimiviruses that infect the protist Acanthamoeba and that are themselves infected by the virophage Sputnik. This paper examines the evolutionary dynamics of this system, using mathematical models. While the models suggest that the virophage population will evolve to increasing degrees of giant virus inhibition, it further suggests that this renders the virophage population prone to extinction due to dynamic instabilities over wide parameter ranges. Implications and conditions required to avoid extinction are discussed. Another interesting result is that virophage presence can fundamentally alter the evolutionary course of the giant virus. While the giant virus is predicted to evolve towards increasing its basic reproductive ratio in the absence of the virophage, the opposite is true its presence. Therefore, virophages can not only benefit the host population directly by inhibiting the giant viruses, but also indirectly by causing giant viruses to evolve towards weaker phenotypes. Experimental tests for this model are suggested

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

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