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Giant Viruses

The recent discovery of really, really big viruses is changing views about the nature of viruses and the history of life

James L. Van Etten

2011-07VanEttenF1.jpgClick to Enlarge ImageThe common view of viruses, mostly true, is of tiny burglars that sneak into cells, grab the biosynthetic controls and compel the cell to make huge numbers of progeny that break out of the cell and keep the replication cycle going. Viruses are supposed to be diminutive even compared to cells that are just a micrometer (1,000 nanometers) in diameter. They are supposed to travel light, making do with just a few well-adapted genes.

In 1992, a new microorganism was isolated from a power-plant cooling tower in Bradford, England, where Timothy Robotham, a microbiologist at Leeds Public Health Laboratory, was seeking the causative agent of a local pneumonia outbreak. His search led to the warm waters of the cooling tower, a known reservoir for bacterial pathogens in the Legionella genus, which are the cause of the pneumonialike Legionnaire’s disease. Particles present in the sample were mistakenly identified as bacteria. Gram positive and visible under the microscope as pathogens within the particle-gobbling amoeba Acanthamoeba polyphaga, the entities surprisingly did not generate any product from the gene-amplifying polymerase chain reaction technique using universal bacterial primers.

2011-07VanEttenF2.jpgClick to Enlarge ImageEleven years later, in 2003, the mystery organism received a new identity and a new name, Acanthamoeba polyphaga Mimivirus, for microbe-mimicking virus. Mimivirus is the largest virus ever discovered. Giant viruses had been known for a few years, many of them in a group termed nucleo-cytoplasmic large DNA viruses (NCLDVs). This group features several other virus families, including Poxviridae, which infects vertebrates (for example, smallpox virus) and invertebrates, the aquatic viruses Iridoviridae and Phycodnaviridae, and the vertebrate virus Asfarviridae. Giant viruses are considered to be ones with genomes larger than 300 kilobase pairs and with capsid diameters of about 200 nanometers or more.

2011-07VanEttenF3.jpgClick to Enlarge ImageMimivirus is a giant among giant viruses, with a diameter of 750 nanometers. It possesses a genome, truly outsized by viral standards, of 1.2 million base pairs, coding an outlandish 1,018 genes. For comparison, the smallest free-living bacterium, Mycoplasma genitalium, is just 450 nanometers in diameter and possesses a genome half the size of that in mimivirus, while coding just 482 proteins. The record tiniest cellular organism, Hodgkinia cicadicola, a parasite in cicadas that was described in 2009, has a genome of just 140,000 base pairs, coding a paltry 169 proteins. H. cicadicola is unable to live on its own, being entirely dependent on the lush environment of specialized cicada cells. Viruses are generally not considered living organisms (although for a consideration of their position in the phylogenetic tree of life, see the sidebar box in the section headed "Origins"), yet mimivirus brings a bigger blueprint and more lumber to the replication process than the living H. cicadicola and many other bacteria.

Most giant viruses have only been discovered and characterized in the past few years. There are several reasons why these striking biological entities remained undetected for so long. Among the most consequential is that the classic tool for isolating virus particles is filtration through filters with pores of 200 nanometers. With viruses all but defined as replicating particles that occur in the filtrate of this treatment, giant viruses were undetected over generations of virology research. (Mimivirus disrupted this evasion tactic by being so large it was visible under a light microscope.) Standard plaquing procedures failed to report the presence of giant viruses because the large particles bogged down in the soft agar of the plaquing medium, disrupting diffusion and the formation of visible plaques. An additional explanation for the elusiveness of the largest viruses is that many infect protists, which have received far less research attention than plants and animals.

With the spotlight finally on them, the giant viruses are delivering striking lessons in viral physiology and ecology, not to mention challenging long-held assumptions about the shape of the phylogenetic tree of life.

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