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Pimp My Virus: Ocean Edition

The views expressed are those of the author and are not necessarily those of Scientific American.


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Image: The starfish-shaped EZ-open structure of mimivirus, above, and the gray DNA-containing nucleocapsid inside, below. The nucleocapsid has plenty of room to breathe and a concave depression, not unlike the dimple on the Death Star, that always faces the "starfish". From PLoS Biology.

In 1992, scientists sampled the water from a cooling tower in Bradford, England, where an outbreak of pneumonia had just occurred. They were looking for respiratory disease-causing bacteria of the sort that cause Legionnaires’ Disease, and they found several, including a new one they named Bradfordcoccus. Except Bradfordcoccus was not a bacterium. Bradfordcoccus, once outed more than 10 years later, would become on its discovery the world’s largest known virus, an entire order of magnitude larger than any known before.

And what a virus it is. Its genome is over 1.1 million base pairs long, which is bigger than that of about two dozen cellular clades, and it codes for over 900 genes, which includes most of the proteins the virus needs to survive. That also means that, according to some scientists, it may be the descendant of some of the earliest life on earth – or sort-of life, anyway.

Its overall shape is one of the few standard things about it: a familiar viral icosahedron – which was the way it was finally identified – encased in a shaggy coat of fibers, which some other viruses do have.But unlike economy viruses whose contents are packed in about as tightly as they can go, the roomy interior houses ample space for a membrane-bound bag containing the organism’s DNA (the nucleocapsid). And it possesses an unique starfish-shaped seal on one of its icosahedral vertices, likely the viral equivalent of the pop top.

They are as big as common bacteria like Rickettsia (one species of which causes Rocky Mountain Spotted Fever), and bigger than Mycoplasma genitalium, the smallest-known free living bacterium (whose own genome is only half as long as mimivirus’s at about 600kb) an organism scientists recently synthesized in the lab in their pursuit of synthetic life. You could almost see one of these things under a light microscope – they’re about 750 nm wide when you include their furry coat. When I took microbiology in college, I could easily see bacteria 1-2 micrometers big under oil-immersion light microscopy.

Image: Mimivirus. Credit: Creative Commons Xanthine

As may be imagined, these viruses are mind-benders for your basic definition of "What Is Alive", to which viruses have traditionally been considered "Most Definitely Not". Though they reproduce, viruses cannot do so without their host cells. And most known viruses are tremendously smaller than their host and depend on them for nearly all of the machinery they need to reproduce. The DNA of giant viruses contain instructions for many of the genes needed to make DNA, RNA, proteins, and sugars that are typically only found in living cells – just about everything they need to reproduce.

French scientists dubbed the entity "mimivirus", for "mimicking microbe". Others called them "giant viruses." And now that scientists have started looking for them, they are finding them all over the planet. It turns out the ocean is full of them.

In October, scientists announced the discovery of a mimi-like virus pulled out of the waters off Texas (you know what they say: "Everything’s Bigger in the Waters Off Texas") parasitizing not freshwater amoebae, but an oceanic predatory protist. This particular new virus (delightfully) attacks a marine microbe called Cafeteria roenbergensis (Proposed new viral targets: Coffeeshopia starbucksii and Buffet allyoucaneatensis) that is a major player in marine food webs, ocean carbon cycling, and the works. The big implication, of course, is that since Cafeteria roenbergensis is, as may be inferred from its name, a robust planktonic predator which may even be the most numerically abundant predator on the planet (PDF), a virus that affects its population dynamics could have a big influence on the whole ocean system. And we didn’t even know it was there.

Image: Cafeteria roenbergensis: Credit: Creative Commons Dennis Barthel/zapyon.

Though the C. roenbergensis virus (which researchers have dubbed CroV) is clearly related to the Acanthamoeba mimivirus (it’s in the nucleocytoplasmic large DNA virus (NCLDV) group, whose other celebrities include the pox viruses and phycodnaviruses of algae), this new virus is substantially different. Less than one-third of its genes clearly share an evolutionary origin with mimivirus genes.

With a genome of 730,000 bp, CroV is the largest known marine virus (probably because it’s the only known marine giant virus). Unlike some of the smallest viruses, which get by on ten or so genes sometimes written over each other on the opposite sides of the same piece of genetic material*, CroV is bursting with goodies, including 544 predicted genes, of which 22 code for transfer RNAs. Transfer RNA (tRNA) shuttles amino acids to messenger RNA – the code for making proteins – in ribosomes during protein synthesis. Considering there are only about 20-22 amino acids needed to make proteins by most organisms, it could theoretically make them all (on the other hand, humans have genes for several hundred kinds of tRNAs. Efficiency, as it has been well documented, is not our genome’s strong suit).

Also unlike many smaller viruses, who actually exploit their genetic sloppiness for evolutionary advantage, CroV, like most cellular organisms, cares about and takes care of its DNA. It encodes its own DNA repair enzymes, among which are two photolyases, which repair damage to DNA from ultraviolet light. There’s also a 38-kilobase region that seems to have come from bacteria, and includes an entire pathway for making a key component of the outer membrane of Gram-negative bacteria. What’s that doing there? It gets weirder: Acanthamoeba mimivirus even contains eukaryotic genes, that is, genes from multicellular or more complex organisms with nuclei like protists. Likely, the viruses picked up their genetic bounty by accident when self-assembling inside a cell and the remains of one of their host’s latest meals or other parasites happened to float by, a process scientists like to call considerably less excitingly "horizontal gene transfer".

Why are these viruses so big? Mimivirus’s large size, it turns out, may be its way of saying "Eat Me" to amoebae. Experiments with precisely sized plastic beads have shown that if mimivirus were any smaller, the amoeba could not engulf them as quickly or effeciently. That may also be true of the predatory Cafeteria. And it may be that by being big, that allowed their genomes to expand further. Of course, being big comes with some costs, too. A mimivirus relative that proved to be even bigger – the "mamavirus", discovered in a water cooling tower in Paris — is the first known virus to have attracted its own parasite: Sputnik virus. Other viruses have been known to have "satellite viruses" that cannot replicate except in their presence. But they incur no fitness cost to their "host" virus. Sputnik (literally, "satellite" in Russian), on the other hand, actively taxes the mamavirus’s ability to replicate, causing it to churn out deformed virions with abnormal capsids, or shells. That is a first. When, as a virus, you have spawned your own viral parasite, you know you have made it, er, big.

For me, the magic of this finding is that we were literally surrounded by these things, and no one knew they were there. Undoubtedly, scientists say, CroV is but the tip of the iceberg for giant viruses in the ocean. Here is the forehead-smacking realization: filters we were using to sift "bacteria"-sized particles from our "viral" samples caught these viruses too, of course. When researchers sampled the "bacterial" fraction of seawater filtrates for NCLDV DNA, 86% tested positive for mimivirus. Untold weirdness awaits.

————————————————————————-

*That is, reading the same piece of DNA or RNA one way you get one protein, and reading part of the same exact piece in the opposite direction yields another. Crazy, but I seem to recall this is true from college virology but can’t find confirmation online. Readers?

References:

Online:

A Giant Among Giants. Small Things Considered, July 26, 2010. Accessed Dec. 20, 2010.

A virus’s virus. The Scientist, Aug. 6, 2008. Accessed Dec. 20, 2010.

Mimivirus: Discovery of a Giant Virus. Accessed Dec. 20, 2010.

Unintelligent Design. Discover Magazine, March 15, 2006. Accessed Dec. 20, 2010.

‘Virophage’ suggests viruses are alive. Nature 454, 677 (7 August 2008) | :10.1038/454677a; Published online 6 August 2008

Viral Missing Link Caught on Film. Wired Science, May 5, 2009. Accessed Dec. 20, 2010.

World’s Largest, Most Complex Marine Virus Is Major Player in Ocean Ecosystems Science Daily, Oct. 31, 2010. Accessed Dec. 20, 2010.

Journal:

Baldauf, S.L. (2008)."An overview of the phylogeny and diversity of eukaryotes". Journal of Systematics and Evolution 46 (3): 263–273. doi:10.3724/SP.J.1002.2008.08060 .

Fischer, M. G.; Allen, M. J.; Wilson, W. H.; Suttle, C. A. (2010). "Giant virus with a remarkable complement of genes infects marine zooplankton". Proceedings of the National Academy of Sciences. doi:10.1073/pnas.1007615107

Matthias G. Fischer, Michael J. Allen, William H. Wilson, Curtis A. Suttle. Giant virus with a remarkable complement of genes infects marine zooplankton. Proceedings of the National Academy of Sciences, 2010; DOI: 10.1073/pnas.1007615107

Xiao C, Kuznetsov YG, Sun S, Hafenstein SL, Kostyuchenko VA, et al. (2009) 1000092Structural Studies of the Giant Mimivirus. PLoS Biol 7(4): e1000092. doi:10.1371/journal.pbio.

For Further Info:

Cafeteria roenbergensis. Wikipedia – With possible interesting story on the origin of the name "Cafeteria". Could not verify because journal wanted to charge me $20 to read the article.

Dare RK, Chittaganpitch M, Erdman DD. Screening pneumonia patients for mimivirus. Emerg Infect Dis [serial on the Internet]. 2008 Mar. Accessed Dec. 20, 2010.

Mimivirus. MicrobiologyBytes, Sept. 11, 2007. Accessed Dec. 20, 2010.

Mycoplasma genitalium. Wikipedia. Accessed, Dec. 20, 2010.

Mimivirus. Wikipedia. Accessed Dec. 20, 2010.

First Virophage Could Take the Fight to Viruses. New Scientist, Aug. 6, 2008. Accessed Dec. 20, 2010.

Even Viruses Get the Blues. Wired Science, Aug. 6, 2008. Accessed Dec. 20, 2010.

About The Author: Jennifer Frazer is a biodiversity blogger and AAAS Science Journalism Award-winning science writer who has written for the Wyoming Tribune-Eagle, The Boston Globe, The (Louisville) Courier-Journal, High Country News, and Fungi Magazine. She holds two biology degrees from Cornell University and a Master’s Degree in science writing from MIT. She writes about the spectrum of life on Earth at her blog, The Artful Amoeba, and tweets (occasionally) at @JenniferFrazer. Like David St. Hubbins, she is concerned about the potential world domination plans of slime molds.

 

The views expressed are those of the author and are not necessarily those of Scientific American.






Comments 3 Comments

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  1. 1. Merry Youle 2:50 pm 12/22/2010

    Hi, Jennifer,

    Thanks for quoting from my Small Things Considered blog post about these giant viruses—one of my favorite topics. I do wish I could take credit for the term "stargate’ as it is so perfect, but I had found it in this paper by Zauberman and colleagues:

    http://dx.plos.org/10.1371/journal.pbio.0060114

    The images there are stunning!

    Merry

    Link to this
  2. 2. QuantaUniverse.com 9:21 pm 12/22/2010

    How do we identify the highest known form of life to exist? Can we rank viruses, bacteria, and parasites by or at their level of existence, the lowest rank being the most "defiled" way of life that we observe?

    Link to this
  3. 3. Jennifer Frazer 11:21 pm 12/23/2010

    Hi Merry,
    Thanks for the clarification and the link. You are right — the photos are amazing! I love the one of the burst capsid where the star-seal has opened. It looks like a seed pod that has dehisced. Convergent evolution strikes again, I’m afraid.

    As for "ranking" life, I don’t think that’s a terribly worthwhile pursuit. Just because bacteria are smaller than us doesn’t mean they don’t have complex lifestyles and capabilities we lack (like living in boiling acid, for instance, or surviving on a diet of heavy metals). I will concede, however, that our ability to produce language, art, tools, and hair metal does give H. sapiens a certain gravitas that E. coli lacks . . .

    Link to this

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