ScienceDaily (Jan. 26, 2012) — MIT
researchers have discovered that certain photosynthetic ocean
bacteria need to beware of viruses bearing gifts: These viruses
are really con artists carrying genetic material taken from
their previous bacterial hosts that tricks the new host into
using its own machinery to activate the genes, a process never
before documented in any virus-bacteria relationship.

The con occurs when a grifter virus injects its DNA into a
bacterium living in a phosphorus-starved region of the ocean.
Such bacteria, stressed by the lack of phosphorus (which they
use as a nutrient), have their phosphorus-gathering machinery
in high gear. The virus senses the host's stress and offers
what seems like a helping hand: bacterial genes nearly
identical to the host's own that enable the host to gather more
phosphorus. The host uses those genes, -- but the additional
phosphorus goes primarily toward supporting the virus'
replication of its own DNA.

Once that process is complete (about 10 hours after infection),
the virus explodes its host, releasing progeny viruses back
into the ocean where they can invade other bacteria and repeat
this process. The additional phosphorus-gathering genes
provided by the virus keep its reproduction cycle on schedule.

In essence, the virus (or phage) is co-opting a very
sophisticated component of the host's regulatory machinery to
enhance its own reproduction -- something never before
documented in a virus-bacteria relationship.

"This is the first demonstration of a virus of any kind -- even
those heavily studied in biomedical research -- exploiting this
kind of regulatory machinery in a host cell, and it has evolved
in response to the extreme selection pressures of phosphorus
limitation in many parts of the global oceans," says Sallie
(Penny) W. Chisholm, a professor of civil and environmental
engineering (CEE) and biology at MIT, who is principal
investigator of the research and co-author of a paper published
in the Jan. 24 issue of Current Biology. "The phage
have evolved the capability to sense the degree of phosphorus
stress in the host they're infecting and have captured, over
evolutionary time, some components of the bacteria's machinery
to overcome the limitation."

Chisholm and co-author Qinglu Zeng, a CEE postdoc, performed
this research using the bacterium Prochlorococcus and its close
relative, Synechococcus, which together produce about a sixth
of the oxygen in Earth's atmosphere. Prochlorococcus is about
one micron in diameter and can reach densities of up to 100
million per liter of seawater; Synechococcus is only slightly
larger and a bit less abundant. The viruses that attack both
bacteria, called cyanophages, are even more populous.

The bacterial mechanism in play is called a two-component
regulatory system, which refers to the microbe's ability to
sense and respond to external environmental conditions. This
system prompts the bacteria to produce extra proteins that bind
to phosphorus and bring it into the cell. The gene carried by
the virus encodes this same protein.

"Both the phage and bacterial host have the genes that produce
the phosphorus-binding proteins, and we found they can both be
up-regulated by the host's two-component regulatory system,"
says Zeng. "The positive side of infection for bacteria is that
they will obtain more phosphorus binders from the phage and
maybe more phosphorus, although the bacteria are dying and the
phage is actually using the phosphorus for its own ends."

In 2010, Chisholm and Maureen Coleman, now an assistant
professor at the University of Chicago, demonstrated that the
populations of Prochlorococcus living in the Atlantic Ocean had
adapted to the phosphorus limitations of that environment by
developing more genes specifically related to the scavenging of
phosphorus. This proved to be the sole difference between those
populations and their counterparts living in the Pacific Ocean,
which is richer in phosphorus, indicating that the variation is
the result of evolutionary adaptation to the environment.

The new research indicates that the phage that infect these
bacteria have evolved right along with their hosts.

"These viruses -- the most abundant class of viruses that
infect Prochlorococcus -- have acquired genes for a metabolic
pathway from their host cells," says Professor David Shub a
biologist at the State University of New York at Albany. "These
sorts of genes are usually tightly regulated in bacteria, that
is they are turned into RNA and protein only when needed by the
cell. However, genes of these kinds in viruses tend to be used
in a strictly programmed manner, unresponsive to changes in the
environment. Now Zeng and Chisholm have shown that these
particular viral genes are regulated by the amount of phosphate
in their environment, and also that they use the regulatory
proteins already present in their host cells at the time of
infection. The significance of this paper is the revelation of
a very close evolutionary interrelationship between this
particular bacterium and the viruses that seek to destroy it."

"We've come to think of this whole system as another bit of
evidence for the incredible intimacy of the relationship of
phage and host," says Chisholm, whose next steps are to explore
the functions of all of the genes these marine phage have
acquired from host cells to learn more about the selective
pressures that are unique to the phage-host interactions in the
open oceans. "Most of what we understand about phage and
bacteria has come from model microorganisms used in biomedical
research," says Chisholm. "The environment of the human body is
dramatically different from that of the open oceans, and these
oceanic phage have much to teach us about fundamental
biological processes."

This research was supported in part by the Gordon and Betty
Moore Foundation, the National Science Foundation's (NSF) CMORE
program, the NSF Biological Oceanography program and the U.S.
Department of Energy.

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The above story is reprinted from materials provided by
Massachusetts Institute of
Technology, Department of Civil and Environmental
Engineering. The original article was
written by Denise Brehm.

Note: Materials may be edited for content and length. For
further information, please contact the source cited
above.

Journal Reference:

Qinglu Zeng, Sallie W. Chisholm. Marine
Viruses Exploit Their Host's Two-Component Regulatory System in
Response to Resource Limitation. Current
Biology, 2012; DOI: 10.1016/j.cub.2011.11.055

Note: If no author is given, the source is cited
instead.

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