A Gazillion Tiny Avatars
By OLIVIA JUDSON
As I mentioned last week, next year is to be the International Year of Biodiversity. So I thought I’d kick
off the celebrations by looking at some of the funkiest beings on the planet: viruses. Viruses have a bad
reputation: in humans, they cause illnesses as varied as colds, flu, cervical cancer, polio and ebola. But to
focus exclusively on the harm they cause is to do them an injustice, for viruses are also fascinating,
mysterious and powerful forces of nature.
First things first: what is a virus?
Viruses are different from all other life forms. Whereas the rest of us — whether we’re talking humans,
mushrooms, petunias or bacteria — are made of one or more cells, viruses are not. They haven’t got a
cell, with all that machinery for detecting, and interacting with, the outside world. Instead, viruses are just
sets of genes packed inside a capsule, or “capsid,” that is usually made out of protein molecules.
(Depending on the virus, the capsid will take one of a number of forms. Some look like 20-sided dice.
Others resemble moon landers — tiny containers on a set of legs.)
Many viruses have unorthodox genetics: instead of using DNA to store their genetic information, they
use a related molecule, RNA. Moreover, while in its capsid, a virus is inert: it does not eat, it does not
breathe. And all viruses are parasites. That is, they cannot reproduce — make more viruses — unless they
are within the cell of a “proper” organism. I say “proper” because many people argue that viruses aren’t
alive, that they mark the boundary between living and non-living. And it is true that they don’t fit into the
tree of life — that map of ancestry by which the rest of us can trace our lineages back to LUCA, the last
universal common ancestor. (LUCA is the being to which all living organisms can, in principle, trace
their family trees.) The tree of life only covers cell-based life forms.
An ability to resist viral attack has sculpted the genomes of all known organisms, from bacteria to
humans. Indeed, the origins of viruses are shrouded in mystery. Are most viruses descended from a virus
that appeared long ago, the viral version of LUCA? (This would give viruses their own tree of life.) Or
have viruses originated several, even many, times during the history of life? No one knows. Despite these
difficulties, I put viruses among the living, myself, on the grounds that they are discrete entities that
reproduce, mutate, experience natural selection and evolve, just as the rest of us do.
But whether you count viruses as living or not, there’s an awfully large number of them: a single drop of
seawater may contain more than 10 million viral particles. That’s more than 10 billion in a liter (two-anda-bit pints) of ocean. Some people have estimated that, in the oceans, there’s more carbon stashed away in
viruses than there would be in 75 million blue whales.
Moreover, viruses are extremely diverse; there are zillions of different kinds. Some, such as MS2, a virus
that attacks bacteria like Escherichia coli, have as few as four genes. Others, such as the gargantuan
Mimivirus, have more than 900. (Mimivirus mostly attacks amoebae, although it is also suspected of
occasionally causing pneumonia in humans.) And each time we look in a new place, we find more and
more viruses that are different from those we have known before.
Fortunately for us, most viruses don’t attack humans; they attack bacteria and other microbes, which they
kill on a colossal scale. In the oceans alone, viruses are reckoned to kill about 100 million metric-tons’worth of microbes every minute. One hundred million metric tons! Given that a typical bacterium only
weighs a tiny, tiny fraction of a gram (and there are a million grams in a ton), that is one huge number of
dead microbes. (For anyone who doesn’t use the metric system, one metric ton is a little bigger than the
American short ton; there are just over 28 grams in an ounce.)
Viruses are thus important, if tiny, avatars of the grim reaper. Which has several interesting
consequences. One is that viruses play a fundamental role in regulating the food chain. This is because
death-by-virus is different from death-by-predator. When a predator kills a microbe, it consumes it: the
microbe’s cell is incorporated into the predator’s body. In contrast, when a virus kills a microbe, the
microbe’s cell bursts open, or “lyses,” releasing new viruses and a lot of cellular debris back into the
environment. This debris can then be consumed by other microbes. In other words, by lysing their
victims, viruses are constantly making food available to other life forms.
A second consequence of all this viral activity is the role viruses play in evolution. An ability to resist
viral attack has sculpted the genomes of all known organisms, from bacteria to humans. (Why, then, do
viruses remain dangerous? The answer to this is complex, but part of the reason is that they are often able
to stay one step ahead of their hosts, because viruses tend to evolve very fast. So if the host evolves a new
way to detect and disable an intruder, sooner or later the virus will evolve a new way to evade the trap.
This is one reason viral diseases are so hard for us to treat.)
But here’s what I find most interesting of all. Viruses don’t just cause other organisms to evolve. They are
also important sources of new genes. The reason is that as viruses move in and out of host cells, they
sometimes take a few host genes with them, or leave some of their own behind. Thus, although viruses
are among the most destructive forces of nature, they are also among the most potent forces of creation.
As you lie in bed with flu, or sit at your desk sneezing with a cold, it may be hard to appreciate the
wonder of viruses. Yet, just as much of the beauty we see around us — the length of a hummingbird’s
beak, the speed of the gazelle — is an evolved response to other life forms (the depth of a flower, the leap
of a cheetah), so too at the level of the cell, much of the intricacy we see is due to evolution in response to
viruses. It’s an intricacy that we are still unraveling: we have much to learn in the years ahead. Perhaps
one day, we’ll be able to use our knowledge to beat viruses at their own game.
Notes:
It is surprisingly difficult to write a water-tight definition of life. But for a vigorous attack on the idea that
viruses
count as living, see Moreira, D. and López-García, P. 2009. “Ten reasons to exclude viruses from the
tree of life.”
Nature Reviews Microbiology 7: 306-311. These authors also provide a historical overview of definitions
of life;
they argue against a single-common ancestor of all viruses. For an alternative opinion of whether viruses
are
alive, see Brüssow, H. 2009. “The not so universal tree of life or the place of viruses in the living world.”
Philosophical Transactions of the Royal Society of London B 364: 2263-2274. For the view that viruses
are
ancient and have their own tree of life, see Forterre, P. and Prangishvili, D. 2009. “The origin of
viruses.”
Research in Microbiology 160: 466-472; see also Filée, J., Forterre, P. and Laurent, J. 2003. “The role
played by
viruses in the evolution of their hosts: a view based on informational protein phylogenies.” Research in
Microbiology 154: 237-243. These authors also provide data showing that viruses are important sources
of new
genes for cell-based life forms.
When I say a “drop” of seawater, I am using that as shorthand for a milliliter — which is around a fifth
of a
teaspoon. For viral abundance in the oceans, and for the estimate that marine viruses are equivalent to
75 million
blue whales, see Suttle, C. A. 2005. “Viruses in the sea.” Nature 437: 356-361; this paper also includes
an
interesting discussion of how death by virus is different from death by predator. For the estimate that
viruses kill
100 million metric tons of microbes in the ocean every minute, see Rohwer, F., Prangishvili, D. and
Lindell, D.
2009. “Role of viruses in the environment.” Environmental Microbiology 11: 2771-2774. For an
excellent review
of the importance of marine viruses, see Fuhrman, J. A. 1999. “Marine viruses and their biogeochemical
and
ecological effects.” Nature 399: 541-548.
For the small genome of MS2, see Fiers, W. et al. 1976. “Complete nucleotide sequence of bacteriophage
MS2
RNA: primary and secondary structure of replicase gene.” Nature 260: 500-507. For the giant genome of
mimivirus, see Raoult, D. et al. 2004. “The 1.2-megabase genome sequence of Mimivirus.” Science 306:
1344-1350. For the role of Mimivirus in pneumonia, see Raoult, D., La Scola, B. and Birtles, R. 2007.
“The
discovery and characterization of Mimivirus, the largest known virus and putative pneumonia agent.”
Clinical
Infectious Diseases 45: 95-102. For an example of novel viruses from novel environments, see LópezBueno, A. et
al. 2009. “High diversity of the viral community from an Antarctic lake.” Science 326: 858-861.
For an interesting discussion of the evolution and counter-evolution between bacteria and viruses, see
Comeau,
A. M. and Krisch, H. M. 2005. “War is peace — dispatches from the bacterial and phage killing fields.”
Current
Opinion in Microbiology 8: 488-494. For viruses shuffling genes to and from bacteria, see for example,
Lindell,
D. et al. 2007. “Genome-wide expression dynamics of a marine virus and host reveal features of coevolution.”
Nature 449: 83-86; Lindell, D. et al. 2004. “Transfer of photosynthesis genes to and from
Prochlorococcus
viruses.” Proceedings of the National Academy of Sciences, USA 101: 11013-11018; and Canchaya, C.
et al.
2003. “Prophage genomics.” Microbiology and Molecular Biology Reviews 67: 238-276.
Many thanks to Dan Haydon and Jonathan Swire for insights, comments and suggestions.