[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

Group action

    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
    higher organisms."

    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
    and cooperate.

    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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