I Contain Multitudes: The Microbes Within Us and a Grander View of Life
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In fact, we are legion, each and every one of us. Always a “we” and never a “me”. Forget Orson Welles, and heed Walt Whitman: “I am large, I contain multitudes.”
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And when animals share habits, their microbiomes often converge. For example, Knight and his colleagues once showed that ant-eating mammals, including pangolins, armadillos, anteaters, aardvarks, and aardwolves (a type of hyena), all have similar gut microbes, even though they have been evolving independently for around 100 million years.
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Our lives are heavily influenced by external forces that are actually inside us, by trillions of things that are separate from us and yet very much a part of us. Scent, health, digestion, development, and dozens of other traits that are supposedly the province of individuals are really the result of a complex negotiation between host and microbes.
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Perhaps it is less that I contain multitudes and more that I am multitudes.
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The little ‘animalcules’ were everywhere.
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This type of partnership gained a new term – symbiosis, from the Greek for ‘together’ and ‘living’.13 The word itself was a neutral one, implying any form of coexistence. If one partner benefited at the expense of the other, it was a parasite (or a pathogen if it caused disease). If it benefited without affecting its host, it was a commensal. If it benefited its host, it was a mutualist. All these styles of coexistence fell under the rubric of symbiosis.
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“The history of warfare always proves more glamorous than accounts of co-operation. Plague, cholera, and yellow [fever] have found their way into the novel, the stage, and the screen, but no one has made a success story of the useful role played by microbes in the intestine or the stomach.”
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When one V. fischeri cell touches the squid, nothing happens. Two cells: still nothing. But if just five cells make contact, they switch on scores of squid genes.
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In other words, microbes sculpt animal bodies.
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An embryo grows, and will continue to do so as long as it gets enough nutrients. The whole sequence seems self-contained, barrelling along like an immensely complicated computer program that runs itself. But the squid and other animals tell us that development is more than this. It progresses using instructions in an animal’s genes, but also in the genes of its microbes. It is the result of an ongoing negotiation – a conversation between several species, only one of which is doing the actual developing. It is the unfolding of an entire ecosystem.
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I think it’s more accurate to see the immune system as a team of rangers in charge of a national park – as ecosystem managers. They must carefully control the numbers of resident species, and expel problematic invaders.
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Others are more sceptical. The most obvious critique, as science writer Emily Willingham puts it, is that “mice don’t have autism, which is a human neurobiological construct shaped in part by social and cultural perceptions of what is considered normal”.
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It was as dramatic a result as Collins could have hoped for: by swapping the bacteria in the animals’ guts, he had also swapped part of their personalities.
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They benefit us. But we shouldn’t let that lure us into a false sense of security. Symbiotic microbes are still their own entities, with their own interests to further and their own evolutionary battles to wage. They can be our partners, but they are not our friends. Even in the most harmonious of symbioses, there is always room for conflict, selfishness, and betrayal.
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So, the world of symbiosis is one in which our allies can disappoint us and our enemies can rally to our side. It’s a world where mutualisms shatter for the matter of a few millimetres.
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The very term symbiosis has been twisted so that its original neutral meaning – “living together” – has been infused with positive spin, and almost flaky connotations of cooperation and harmony.
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Meanwhile, in South America, acacia trees rely on ants to defend them from weeds, pests, and grazers. In return, they give their bodyguards sugary snacks to eat and hollow thorns to live in. It looks like an equitable relationship, until you realise that the tree laces its food with an enzyme that stops the ants from digesting other sources of sugar. The ants are indentured servants. All of these are iconic examples of cooperation, found in textbooks and wildlife documentaries. And each of them is tinged with conflict, manipulation, and deceit.
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When pathogens infect our guts, they almost always begin by latching onto glycans – sugar molecules – on the surface of our intestinal cells. But HMOs bear a striking resemblance to these intestinal glycans, so pathogens sometimes stick to them instead. They act as decoys to draw fire away from a baby’s own cells.
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When animals get sick, we frequently lose our appetite – a sensible tactic that diverts energy from foraging and towards getting better. It also means that our gut microbes experience a temporary famine. Sick mice deal with this problem by releasing emergency rations: a simple sugar called fucose. Gut microbes can snip off this sugar and feed on it, staying alive while they wait for their hosts to resume normal service.
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The problem with antibiotics is less their use than their overuse, which both disrupts our microbiome and foments the rise of antibiotic-resistant bacteria. The solution is not to demonise these drugs but to deploy them judiciously, in situations when they are actually needed and in full knowledge of the risks and benefits.
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Speaking of which, what counts as dysbiosis? How can you tell if an ecosystem is in disarray? A bloom of C. difficile that causes unstoppable diarrhoea is a clear problem, but most other communities are not so easily classified. Is a gut without B. infantis in a state of dysbiosis? If your microbiome has fewer species than a hunter-gatherer’s, is it dysbiotic? The term is great at conveying the ecological nature of disease but it has also become microbiology’s version of art or pornography: hard to define, but you know it when you see it. And many scientists seem unhelpfully quick to label any ...more
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Over a single day, vaginal communities can change dramatically and rapidly, flitting in and out of states that are supposedly conducive to disease, but with neither clear causes nor ill effects. If you tried to determine a woman’s health by analysing her vaginal microbes, the results would be hard to interpret and might be outdated by the time they arrived.
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So, mammalian success was founded on vegetarianism, and that vegetarianism was founded on microbes.
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In other words, microbes shaped the evolution of the mammalian gut, and the shape of the mammalian gut influenced the evolution of microbes.
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As their diets changed, so did the recruits’ microbiomes – and quickly. Within a single day, they could flip between a carbohydrate-busting, plant-eating mode, and a protein-busting, meat-eating one.
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The bacteria in the yoghurt neither colonised the volunteers’ guts, nor changed the composition of their microbiomes. It’s the same problem that Herter and Kendall identified in the 1920s, and that Matthew Becker and others saw when working on probiotics for frogs. They’re like a breeze that blows through two open windows.
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It was almost as if Khoruts had done an organ transplant, throwing out his patient’s diseased and damaged gut microbiome and replacing it with the donor’s shiny new one. This makes the microbiome the only organ that can be replaced without surgery.
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There’s a popular saying among doctors: There’s no such thing as alternative medicine; if it works, it’s just called medicine.
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Within 24 hours of moving into a new place we overwrite it with our own microbes, turning it into a reflection of ourselves. When people invite you to “make yourself at home”, you and they really have no choice in the matter.
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Whether dog or human, all animals live in a world of microbes. And by moving through that world, we change the microbes in it.
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As in the dolphin enclosure and the human gut, perhaps the quest to sterilise our hospitals has created dysbiosis in the microbiomes of our buildings. By removing harmless bacteria that would otherwise impede the growth of pathogens, perhaps we have inadvertently constructed a more dangerous ecosystem.
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Gibbons showed this by studying public toilets.6 He found that thoroughly scrubbed toilets are first colonised by faecal microbes, which are launched into the air by roiling, flushed water. Those species are eventually outcompeted by a diverse range of skin microbes, but once the toilet gets scrubbed again, the communities go back to square one. So, here’s the irony: toilets that are cleaned too often are more likely to be covered in faecal bacteria.
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Almost every architectural design choice affects the microbial ecology of buildings, which could then affect the microbial ecology of us. Or, as Winston Churchill said, “We shape our buildings, and afterwards our buildings shape us.”