FOR sheer numbers, no other ocean beings can match viruses. Thousands,
sometimes even millions of these molecular parasites inhabit every drop of
surface seawater, outnumbering even bacteria by 10 to 1. Yet despite these
numbers, scientists in the infant discipline of marine virology disagree
vehemently over just how important they are to the ocean ecosystem.
Most consider viruses to be a legion of cripples, sterilised by ultraviolet
radiation and rendered impotent by hosts that are largely immune to their
threat. But a few researchers take the opposite view. And if they turn out to be
right, viruses could radically alter the balance of life in the oceans, ripping
away huge parts of the food web that supports whales, sea birds and the
fisheries on which many people rely.
Yet a quick mental reckoning suggests that viruses鈥攎ost of which infect
bacteria, not larger organisms鈥攎ay not be all that important. In
laboratory cultures, a single virus has only about 1 chance in 100 million of
successfully infecting any given bacterium in a millilitre of water during the
course of a day, says Bruce Levin, an expert on the population biology of
viruses from Emory University in Atlanta, Georgia. If this applies in the real
world, then at a density of 100 000 viruses per millilitre鈥攁 moderate
concentration for a single type of virus鈥攐nly about 1 bacterium in 1000
should succumb to viruses each day.
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But even if Levin鈥檚 back-of-the-envelope calculation vastly underestimates
the impact of the viruses, most bacteria will quickly evolve resistance to these
tiny enemies, says John Waterbury of Woods Hole Oceanographic Institution in
Massachusetts. In Woods Hole harbour, for example, Waterbury found that the most
common strains of Synechococcus, an abundant group of cyanobacteria,
were resistant to most of the naturally occurring viruses that attack them. He
found a few strains of Synechococcus that were susceptible to the
common viruses in his samples, but they were rare components of the
cyanobacterial mix.
Most virologists think that this resistance prevents viruses from being a
major cause of death in bacteria. Waterbury estimates that even at Woods Hole
harbour, where the water teems with Synechococcus, only about 2 per
cent succumb to infection. Despite this, he thinks the viruses may drive a
merry-go-round of different bacterial types.
In this scenario, an individual strain becomes common enough to edge over the
threshold at which its viruses spread easily. The number of viral infections
increases, driving that bacterial strain back into obscurity. A different
cyanobacterial strain that is resistant to those viruses, but susceptible to
others, then becomes dominant, and the pattern is repeated. Waterbury is now
developing molecular ID tags that will allow him to recognise individual
cyanobacterial and viral strains, so that he can test this idea.
Even if the bacteria did not grow resistant to their attackers, viruses would
seem to have an uphill struggle to make their mark on the oceans. Many of the
viral particles in seawater are so badly damaged by exposure to sunlight that
they can no longer function. Ultraviolet light that penetrates the upper layers
of the ocean is a serious health hazard for viruses. It breaks their DNA and
forms cross-links between nucleotides. When a damaged virus infects a bacterium
by injecting its DNA, these cross-links prevent the viral DNA from hijacking the
host cell and forcing it to turn out copies of the virus.
In surface waters, more than 99 per cent of all viruses can be inactivated by
UV light every day, says Curtis Suttle, a marine microbiologist at the
University of British Columbia in Vancouver. 鈥淭he water column is sterilised on
a daily basis,鈥� he says.
At first glance, this seems further proof that viruses have only a bit part
to play in the oceans. Yet the latest data from Suttle and his colleagues
suggest that viruses may get round the UV problem by tricking their bacterial
hosts into repairing the damage. Cross-linked viral DNA can easily get inside
bacterial cells; its difficulty is in commandeering the host鈥檚 DNA. And once the
virus is inside, a light-activated bacterial enzyme known as photolyase mistakes
the viral DNA for its own, and innocently repairs it, allowing the resurrected
viruses to go on to kill their host.
鈥淭his process is probably responsible for the maintenance of viral
populations in the sea,鈥� says Suttle. 鈥淚 don鈥檛 think viruses would exist in
surface seawater if it weren鈥檛 for the fact that bacteria are repairing their
顿狈础.鈥�
In an experiment first reported at a conference this summer, Suttle and his
colleagues collected water samples from the Gulf of Mexico just before dawn,
when UV damage should be at a minimum. They separated the bacteria from the much
smaller viruses and exposed half the viruses and half the bacteria to sunlight,
keeping the other half in darkness. Then they mixed bacteria and viruses again
and watched what happened.
As expected, viruses kept in the dark were more infective than those exposed
to light, clear evidence that sunlight cripples the viruses. But the tests also
showed that damaged viruses were much more infective in bacteria that had been
exposed to light, which activates photolyase, than in bacteria kept in the dark.
These results do not prove that photolyase repair is going on, Suttle says,
because the researchers did not measure enzyme activity directly. However, it is
strong circumstantial evidence.
Suttle鈥檚 results fit well with other evidence that suggests that viruses are
a powerful force in the sea, and one that determines how many plankton and
ultimately how many fish, and even humans, an ocean ecosystem can support. Jed
Fuhrman and his graduate student Rachel Noble of the University of Southern
California have tried a three-pronged analysis to estimate how many bacteria
fall prey to viruses in the waters off Los Angeles.
First, they filtered out protozoans鈥攖he other prime predators of
bacteria鈥攆rom water samples and watched to see if bacteria still died.
Then, with the aid of an electron microscope, they looked for fledgling viruses
inside bacterial cells. By Fuhrman鈥檚 estimate, developing viruses are visible
only during the last tenth of their life cycle, just before they burst out of
the cell, so the actual number of viral infections is about ten times the number
of visibly infected cells. And, finally, they used radioactive tracers to
measure the rate at which new virus particles are produced. For every twenty or
so new viruses, they estimated, one bacterial cell must have died.
All three of these measures yielded roughly the same answer: somewhere
between 20 and 60 per cent of marine bacteria die from viral infections. This is
an admittedly broad range, but it is clearly 鈥渕any鈥� rather than the 鈥渇ew鈥�
suggested by virologists鈥� earlier numbers games. Although each of the estimates
is rather shaky on its own, the fact that they all converge on the same result
suggests they are probably correct, says Fuhrman. If so, as many bacteria
succumb to viruses as are consumed by protozoans鈥攁 big surprise for most
oceanographers, who are accustomed to thinking of viruses as bit players.
Other experts remain sceptical about Fuhrman鈥檚 conclusions because of the
uncertainties in his estimates. But if he is right, viruses must have a profound
influence on the entire oceanic ecosystem. When protozoans eat bacteria, energy
passes along the food chain leading from protozoa to other zooplankton to larger
predators, including fish. But when virus-infected bacterial cells burst, their
energy-rich cell contents spill into the water for other bacteria to
scavenge.
鈥淰iruses tend to keep nutrients away from the big stuff and keep them going
around in the little stuff,鈥� says Fuhrman. If so, viruses have shaped the entire
structure of the ecosystem. Without viruses, there would be many more fish in
the sea.