Ailing Virus Draws Scientific Attention

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“The fact that a virus can get sick makes it more alive,” says virologist Jean-Michael Claverie.

Even more remarkable than the identification of a new giant mimivirus was the unexpected discovery that it was infected with and sickened by a previously unknown tiny virus called “Sputnik.” Finding a virus made ill by another virus has rekindled the debate about whether or not viruses are alive or just rogue scraps of genetic code designed to hijack a host’s genome to reproduce.

Mimiviruses Have Been Fascinating Scientists Since They Were First Described in 2003

The first mimivirus, or “mimicking” microbe, because it was initially mistaken for a bacterium, was found infecting an amoeba in a small industrial cooling tower on the outskirts of Bradford, UK by Jean-Michel Claverie and Didier Raoult, virologists from the Université de la Mediterranée in Marseille, France (recently renamed “Aix-Marseille University”).

Close inspection revealed that mimivirus had 900 protein encoding genes, dwarfing the genomes of other viruses and bigger even than some bacteria and archaea. Recent work with a new technique called polyadenylated RNA pyrosequencing has enabled Claverie, Chantal Abergel and their colleagues in Marseille to not only further confirm the presence of these 900 genes but to identify 75 more, bringing the known mimivirus genome up to almost a thousand.

New Strain of Mimivirus Infected By Genetically Bizarre Little Virus Dubbed “Sputnik”

Then, in 2008, Bernard La Scola, Didier Raoult and their collaborators from the Université de la Mediterranée and the United States discovered the new mimivirus in water from a Parisian cooling tower. They called it Acanthamoeba polyphagamimivirus, or AMP, and nicknamed it “mamavirus,” for “mammoth” microbe. While examining their newest giant virus under an electron microscope, the team discovered that mamavirus was infected with a tiny – just 21-gene – virus and named it “Sputnik” after “traveling companion” in Russian.

Whereas mamavirus is a typical mimivirus, Sputnik is an entirely new find. Its genes are a mishmash, borrowed or stolen from an archaeal virus or plasmid, a mimivirus, possibly mamavirus, and a currently undiscovered family of small viruses. “One of Sputnik’s most remarkable characteristics is its apparent chimeric origin which,” says La Scola, “seems to be one of the most convincing cases so far for gene mixing and matching within the virus world.”

Sputnik Needs Mamavirus to Reproduce and Harms it in the Process

When mimiviruses infect amoebae, they hijack their genes to build huge cell-like “viral factories;” replication and assembly centers where new viral particles are made. Sputnik, in turn, pirates the mamaviral factory to make copies of itself. Attempts to culture Sputniks in amoeba cells without mamavirus were unsuccessful, says Claverie but when mamavirus was added, Sputnik multiplied just fine. It was obvious that Sputnik could not replicate without mamavirus.

But while the relationship is good for Sputnik, mamavirus does not fare so well. Sputnik infection results in deformed mamavirus progeny, in other words, it gets sick. “Sputnik thus behaves as a true parasite with a detrimental effect on AMP reproduction,” Claverie stresses. There are satellite viruses, he acknowledges, those that exploit helper viruses. But La Scola argues that Sputnik is more than a satellite virus because it not only uses its partner’s virus factory, it impairs its fitness. They therefore call Sputnik a “virophage.” Like bacteriophages, virophages can harm their hosts but phages also shuttle genes around; thus Sputnik may be an important vector in lateral gene transfer.

Giant Viruses and their Virophages Are Changing Scientific Thinking about Viruses

“After being considered non-living and relegated to the wings by most biologists, viruses are once again center stage,” says Claverie, adding that they might even have played a central role in the invention of the enclosed nucleus, or eukaryotic cell. Moreover, Claverie thinks we’ve been looking at the wrong thing; viruses he says are their factories not the metabolically silent infecting particles. “Interpreting the virion particle as ‘the virus,’ is very much like looking at a spermatozoid and calling it human,” he stresses. The unusual features of giant mimiviruses suggest they are very much alive, and the discovery that some of them get sick adds a new twist to this old debate – which is likely to go on for some time.

Update (21, May 2011)

A second virophage called “Mavirus,” which is short for “Maverick virus,” was recently found infecting the giant marine virus Cafeteria roenbergenis virus (CroV) by Curtis A. Suttle and Matthias G. Fischer from the University of British Columbia, Vancover, Canada and the Max Planck Institute in Heidelberg, Germany respectively. Not only is this new virophage proof that small viruses can parasitize larger viruses, the researchers think that Mavirus represents an evolutionary link between DNA viruses and transposons (jumping genes) in eukaryotes (a group that includes amoebas, yeasts, worms, plants and us all of whom have linear DNA).

References:
Claverie JM. “Viruses take center stage in cellular evolution.” Genome Biology 2006; 7(6): article 110.

La Scola B, Desnues C, Pagnier I, Robert C, et al. The virophage as a unique parasite of the giant mimivirus. Nature 2008; doi: 10.1038/Nature 07218.

Legendre m, Audic S, Poirot O, et al. mRNA Deep Sequencing Reveals 75 New Genes and a Complex Transcriptional Landscape in Mimivirus. Genome Research online, April 1, 2010.

Ogata H, Claverie JM. How to Infect a Mimivirus. Science 2008; 321:1305-1306.

Fischer M.G., Suttle C.A.A Virophage at the origin of Large DNA Transposons. Science 2011; 332:231-233,
This article was originally published on Suite101.

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