Giant viruses in the oceans: the 4th 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 4th 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.


Report
The 4th Algal Virus Workshop http://www.avw4.org organized by Corina Brussaard and Herman Gons, and hosted by the Royal Netherlands Institute for Sea Research, was held in Amsterdam 17-21 april 2005. Though marine ecology rather than basic virology was the main focus of this meeting, exciting new results on the genomics of large/giant viruses kept turning up in many talks. In the context of a comparative study, Corina Brussaard (in collaboration with the US DoE) is herself sequencing a variety of Micromonas pusilla and Phaeocystis globosa dsDNA viruses some of them estimated to have a genome sizes up to 460 kb.
In his overview, Curtis Suttle (University of British Columbia, Vancouver, Canada) pointed out that viruses (including RNA-, DNA-, prokaryotic and eukaryotic viruses) constitute a significant part of the biomass in ocean coastal waters (with up to 50 millions particles/ml, for a total estimate of 25 to 270 Megatons in the oceans) where they play a dominant role in the control of phytoand bacterio-plankton populations, and hence on the production of oxygen and atmospheric dimethylsulphide, an important factor in climate regulation. Most of these viruses are uncharacterized [1].
Ironically, this is in a freshwater unicellular green alga that the best characterized large DNA virus Paramecium bursaria chlorella virus (PBCV-1), the prototype of the Phycodnaviridae, was isolated more than 20 years ago in Jim van Etten's laboratory (University of Nebraska, Lincoln) [2]. Scanning Electron Microscopy picture of Emiliania huxleyi [9]. Alien looking E. huxleyi is the host of phycodnavirus EhV-86, the 407-kb genome of which was sequenced at the Sanger center [10]. Finally, Willie Wilson's group (Plymouth Marine Laboratory, UK) claimed the bronze medal in the fierce competition for genome size [5]. They presented the complete genome sequence of Coccolithovirus EhV-86, a ds-DNA infecting alien-looking calcarous nanoplankton Emiliania huxleyi (Fig. 1). The genome is made of 407,339 bp (40.2% G+C) and encodes 472 putative protein coding regions. Only 66 (14%) of them have recognizable homologues in the public databases. As other giant viruses, EhV-86 exhibits its share of unexpected genes and functions, most notably a number of enzymes involved in the biosynthesis of sphingolipids. Albeit phylogenetically branching at the root of the Phycodnaviridae (e.g. PBCV-1 or EsV), EhV-86 does encode it own DNA-dependent RNA polymerase complex, thus filling the gap with the other Nucleo-Cytoplasmic Large DNA virus families (Irido-, Asfar-, Pox-, and Mimi-viridae) that all exhibit virallyencoded RNA-polymerases. Pending approval by ICTV, EhV-86 might become the prototype of the coccolythovirinae, a new subfamily of phycodnaviridae.
In his closing lecture, Jim Van Etten, reminded the new comers in the field of algal viruses that reports of very large icosahedral virus-like particles in various aquatic and marine organisms can be traced back to the 50's, but failed to elicit much interest outside of the community of marine biologists. The discovery and genome characterization of the large freshwater chlorella viruses [2], and more recently of giant amoeba infecting Mimivirus [6] (remotely related to phycodnaviruses but not an algal virus) elicited a renewed interest in the genomics of these large marine viruses, as they may provide new insight on the early evolution of eukaryotes. Not unexpectedly, close relatives of Mimivirus appear to exist in the marine environment, as suggested by the numerous homologous sequences found by J.-M. Claverie and E. Ghedin (The Institute for Genomic Research, Rockville, USA) in their exhaustive analysis [7] of the Sargasso Sea environmental data set [8].
The 4th Algal Virus Workshop made it clear that these giant algal viruses are now entering the genomic era at full speed. The amount of surprises that we can expect while deciphering their genomes will be as big as their diversity, and more dogma on what a virus should look like will probably be shattered along the way.