[Paleopsych] NS: A billion bacteria brains are better than one
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A billion bacteria brains are better than one
* 20 November 2004
* Mark Buchanan
* Mark Buchanan is a writer based in Cambridge
IN A small dish in a lab at the University of Chicago, millions of
bacteria are deliberating among themselves. For hours there is no
activity then suddenly, having taken a vote and come to a decision,
the bacteria all light up, filling their world with a soft blue glow.
Nearby, other bacteria are navigating as a pack. In response to unseen
signals, individual bacteria have grown tendrils and gathered
together, forming a raft that glides easily over the solid surface.
Extraordinary behaviour for bugs? Biologist Jim Shapiro doesn't think
so. He watches this sort of thing every day in his lab. And he regards
it as yet more evidence that the popular view of microbes is way off
track. For most of the two centuries since scientists first peered
into the microscopic world, they have viewed life's tiniest members as
loners, living individual, independent lives. But Shapiro and other
biologists know that there is no such thing as an antisocial microbe.
Bacteria, amoebas and yeast are not renowned for their social skills,
but Shapiro thinks they should be.
Wherever microbes coexist in rich profusion - which is pretty much
everywhere, from the scum on a pond to a cockroach's gut - teamwork
and cooperation count every bit as much as cut-throat competition. And
behind it all stands a talent for communication that is turning out to
be far more sophisticated than anyone imagined. Bacteria use a
bewildering range of chemical messages not only to attract mates and
distinguish friend from foe, but also to build armies, organise the
division of labour and even commit mass suicide for the good of the
community. Some experts even talk about "microbial language", with its
own lexicon and syntax. That is a radical interpretation, but microbes
are certainly much cleverer than we thought. They are not just stupid
little bags of enzymes, insists Shapiro, but "formidable and
sophisticated actors on the stage of life".
The idea that microbial communities might be intensely social has been
around for about 20 years, but most biologists did not take it too
seriously. In the lab, researchers usually keep microbes as prisoners
in well-stirred suspensions, which prevents them getting together to
form colonies. That is fine for many types of research, but anyone
interested in animal behaviour knows that the only way to get a real
insight into what creatures do is to study them in their natural
And away from the artificial simplicity of the lab, microorganisms
adore surfaces. You'll find them almost anywhere, from the hulls of
boats and the walls of pipes and drains to the surfaces of ponds,
water tanks and living organisms. "Of all the cells that make up the
healthy human body," points out biologist Jim Deacon of the University
of Edinburgh, UK, "more than 99 per cent are microorganisms living on
the skin, in the gut or elsewhere." These surface-dwelling
communities, often containing hundreds of distinct species, are known
as biofilms. The microbes within a biofilm collectively weave a matrix
of sugary polymers called exopolysaccharides that form the physical
infrastructure of a slimy microbial city (New Scientist, 31 August,
1996, p 32). The community living within often has a strength and
integrity its individual citizens lack.
Earlier this year, biologist Staffan Kjelleberg and colleagues at the
University of New South Wales in Australia showed, for example, how
forming a biofilm can enable bacteria to defend themselves against
predators. The versatile bacterium Pseudomonas aeruginosa thrives in
sewage-treatment plants and in the soil, but everywhere it falls prey
to voracious protozoans. "On the surface of a pipe," says Kjelleberg,
"protozoa move just like vacuum cleaners." He and his colleagues found
that colonies of P. aeruginosa could develop into dense biofilms that
were resistant to attack. "They form a structure that protozoa find
hard to eat," says Kjelleberg. In comparison, colonies of mutant
bacteria deficient in the art of biofilm development remained easy
The biofilms in these experiments are extremely rudimentary. Natural
biofilms - in everything from dental plaque to spoilt food - are so
complex that researchers still cannot reproduce their full glory in
the lab. Yet by studying microbes in somewhat simplified settings,
they are peeking into their social lives and learning how they get it
One of the most important techniques microbes use to coordinate
teamwork is known as quorum sensing. In the laboratory of Bonnie
Bassler at Princeton University, a bacterium called Vibrio harveyi
shows how it works. These bacteria routinely produce a molecule known
as an autoinducer, which they release into the environment. The result
under many conditions is precisely nothing. But at a high enough
concentration, the autoinducer triggers a chemical response in other
V. harveyi, making them glow. The concentration of autoinducer
reflects the density of the bacterial population so, when numbers are
high enough, the bacteria will spontaneously light up with a dull blue
So, while V. harveyi will not shine as an individual, it does in a
group. Biologists are not yet sure what it gains by this behaviour,
but many other bacteria perform similar feats, and in some cases
researchers have found out why. Outside the lab, the marine bacterium
V. fischeri - a close relative of V. harveyi - often lives in dense
colonies on the Hawaiian bobtail squid. The squid gives the bacteria a
protected environment in which to multiply and, in return, the
bacteria light up, helping to camouflage the squid in its deep-sea
habitat. When swimming alone in the sea, the bacteria don't bother to
glow - they save their energy.
Biologists discovered the basic logic of quorum sensing in V. fischeri
in the 1980s. Over the past decade, Bassler and others have learned
that most microbes exploit similar tricks. In the lungs of cystic
fibrosis patients, for example, P. aeruginosa uses quorum sensing to
decide when to deploy virulence factors - molecules that ease its
entry into tissues or help it to counter host defences. By relying on
a system that is only triggered into action when a crucial threshold
is reached, the colony avoids stirring up the immune system too early.
Instead it assembles a formidable force before launching the invasion
When threatened with starvation, the soil-dwelling bacterium
Myxococcus xanthus responds with a similarly impressive display of
social coordination. When the concentration of autoinducer reaches a
critical level, many individuals commit what appears to be socially
inspired suicide. The cells disintegrate, releasing raw materials that
ensure the survival of a lucky few. These become quiescent spores
wrapped within a fruiting body formed of less lucky cells, which gives
them a good chance of surviving to germinate when conditions improve.
Hundreds of microbes use quorum sensing, but experiments with V.
harveyi in particular have revealed the potential flexibility of this
communication strategy. Two years ago, Bassler and colleagues
discovered that V. harveyi has not just one quorum-sensing circuit but
two, and uses them in combination, like tools in a carpenter's
workshop, to orchestrate more subtle acts of cooperation.
One of the circuits in V. harveyi triggers light production only when
it senses a quorum of bacteria of the same species. But the second
circuit, operating through a distinct set of autoinducer molecules, is
not so picky. It triggers light production when enough bacteria of any
species happen to be nearby. "It seems paradoxical," says Bassler,
"that these bacteria use two systems when either alone should be
sufficient." But she suggests that having two systems might allow V.
harveyi to modify their behaviour in subtle ways, depending on whether
they are in the minority or the majority in a community of species.
The discovery of quorum sensing and its widespread use in the
microbial world has ushered in a new view of microbes as highly social
creatures. Indeed, the level of cooperation between individuals can be
so complex that they act less like a coordinated group of
single-celled organisms and more like a microbial "superorganism".
Just as multicellular organisms depend on cellular differentiation to
create specialised cells to make muscles and nerves, for example,
microbial colonies do the same. "You look at these biofilms and you
find a lot of differentiation," says Kjelleberg. "They really are like
Shapiro points out that even simple colonies of the same species can
be highly sophisticated, as cells in distinct regions differentiate to
produce what amounts to different tissues. The bacterium Proteus
mirabilis swims easily in a liquid using its few whip-like flagella,
but individuals cannot move over a solid surface. A colony growing on
a surface can, through chemical communication, orchestrate a
collective metamorphosis in which many of the bacteria turn themselves
into elongated cells covered with thousands of flagella, which they
can use to move over the surface. "These cells are sensitive to
touch," says Shapiro, "and they like to line up next to one another."
The resulting raft of specialised bacteria helps the colony to spread
by swarming over surfaces on which ordinary individuals would remain
stuck. The swarming bacteria can later return to the normal condition,
which is more suited to swimming.
Given that quorum sensing allows microbes to talk to one another in
order to cooperate, it is not surprising that some organisms have
learned how to disrupt their enemies' communication systems. As a
saboteur, the bacterium Bacillus subtilis produces a molecule that
modifies the autoinducers used by many other bacteria, thereby ruining
their effectiveness. And the marine red alga Delisea pulchra, common
on the coast of southern Australia, produces chemicals called
furanones. Similar to autoinducers, these molecules effectively swamp
the receptors of microbes' quorum-sensing systems, jamming
communication. "The algae paint their surfaces with these molecules,"
says Kjelleberg, and so defeat microbial attack.
This particular countermeasure turns out to be popular among microbes.
"We have a whole freezer full of organisms that do similar things,"
says Kjelleberg. "There are really a lot of them." Stimulated by this
discovery, he and his colleagues have produced synthetic molecules
that they are trying to develop into new antibacterial drugs. Unlike
conventional antibiotics, these would function not by killing the
individual microbes, but by destroying their ability to communicate
It's not just outsiders that are bent on subverting the teamwork of
social microbes. Sometimes the sabotage comes from within. In any
society where you have individuals cooperating for the good of the
group, you are likely to get freeloaders who refuse to pull their
weight but still enjoy the benefits of being part of a collective.
Microbial societies are no exception. Last year, biologists Gregory
Velicer and Francesca Fiegna of the Max Planck Institute for
Biological Cybernetics in Tübingen, Germany, witnessed the
consequences of cheating in a colony of M. xanthus, which would
ordinarily form a "fruiting body" in response to a crisis. Normally,
it seems to be a lottery as to which individuals sacrifice themselves
and which benefit from the collective response by becoming spores and
passing on their genes to the next generation. But when Velicer and
Fiegna augmented the colony with a few mutant individuals from
populations that could not form fruiting bodies, they found that these
mutants contributed less than the normal bacteria to fruiting-body
formation, and were more likely to become spores.
As well as giving a fascinating insight into the biology of cheating,
the study also throws light on one of the classic puzzles of
evolutionary biology - why cooperation between individuals persists
despite the potential threat from freeloaders. Velicer found that the
mutant bacteria contain the seeds of their own destruction. Because
they greedily push their own genes into the next generation, the
freeloaders proliferated rapidly in the community, displacing
cooperators. This outbreak of cheating eventually led to a dramatic
population crash, and in some cases the colony perished entirely. This
isn't an ideal outcome for anyone, and it is likely that microbes have
evolved ways to police cheating and preserve cooperation.
How cheaters could be stymied remains a mystery. Velicer points out
that a society of microbes might direct extra benefits to those who
don't cheat, or might directly punish cheaters. This would probably
entail forms of communication that are so far unknown. But he is
hopeful of finding them, given the great progress in uncovering the
vast and complex world of microbial communication. Velicer is
certainly not alone in his belief that there is much more to be
discovered about microbial communication. "We fully expect that this
is merely the tip of the iceberg," says physicist Eshel Ben-Jacob of
Tel Aviv University in Israel.
What's more, if Ben-Jacob is correct, microbial communication is more
than just an intricate exchange of chemical messages. He believes it
is something akin to language. In a recent article, he and his
colleagues argue that when other researchers talk about the "syntax"
of microbial signals, or their "contextual" meaning, they should
consider the possibility that this is more than a metaphor (Trends in
Microbiology, 2004, vol 12, p 366).
Words and meanings
Microbial signals are like a real language, they argue, in that they
represent "words" whose meaning can differ in different contexts. As
with human language, bacteria possess a lexicon, or vocabulary, of
possible signals with which to communicate the various signaling
chemicals they produce and recognise, such as those used in quorum
sensing. And the meaning conveyed through these signals depends
strongly on the semantic context. Bacteria carry internal information
reflecting their history as well as current external conditions, and
can respond to the same signal in different ways at different times,
showing a rich behavioural repertoire.
Ben-Jacob's interest in microbes indicates a changing attitude towards
Earth's smallest inhabitants. At last people are waking up to the fact
that most of life is microscopic, and that the macroscopic bits
wouldn't be what they are without microbes. The discovery that these
two worlds have much more in common than we thought is intriguing.
More and more researchers agree with Ben-Jacob's assertion that
microbes have the kind of social intelligence previously considered to
be the exclusive preserve of the most intelligent animals.
Microorganisms recognise the social groups to which they belong, and
readily pick out strangers who might pose a threat.
As we find out more, we will perhaps perceive microbes as more like
ourselves, or discover the roots of our own social behaviour in the
supposedly "simple" microbial world. Perhaps our own ability to talk
and communicate, to form teams and root out and punish freeloaders,
goes all the way back to our days as bacteria.
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