I Contain Multitudes: The Microbes Within Us and a Grander View of Life
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These acts of transmission, where animals hand microbes to their offspring in a generational relay, are among the most critical in the world of symbiosis, because they braid together the fates of hosts and symbionts.8 They ensure that the long waltz is actually long, that it continues through time, that new generations of animals and microbes will take hold just as their parents did.
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When a baby koala is six months old, it weans off its mother’s milk and moves on to eucalyptus leaves. But first, it nuzzles mum’s backside. She, in response, releases a fluid called pap, which the joey swallows.
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pap with bacteria to allow joey to digest the leaves
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Termites, in the words of Greg Hurst, ‘go in for anal-licking, or proctodeal trophollaxis to give it its posh name’. Like koalas, they need microbes to digest their food – in this case, wood – and they get theirs by sucking fluid from their relatives. But, unlike koalas, termites lose the lining of their guts, and all the microbes within, every time they moult their outer shells. So they regularly need to lick their sisters’ backsides to replenish their supply. We might find these habits unsavoury, but we are unusual in our distaste.
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Many familiar animals, including cows, elephants, pandas, gorillas, rats, rabbits, dogs, iguanas, burying beetles, cockroaches, and flies, regularly eat
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feces
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a practice known as coprophagy.
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coprophagy
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Lombardo simply thinks that microbial transmission is another plausible benefit, and one that is traditionally ignored. When people think about contagious microbes, they tend to think of pathogens first. Herds, flocks, and colonies make it easier for diseases to spread. But they also create opportunities for beneficial symbionts to find new hosts.
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The seemingly infinite range of transmission routes through which animals pick up microbes from one another all serve the same imperative: the need to move microbes from one generation of hosts to the next.
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Would a zebrafish just accept a mouse’s gut microbes, and vice versa? The answer was yes. But Rawls found that the animals didn’t just stick with the hands they were dealt. Instead, they reshaped their new communities to more closely match their native ones. The mice partly mousified the fish microbiomes, and vice versa.
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random chance lords over the whole production, which is why even genetically identical mice that live in the same cage end up with slightly different microbiomes.
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Endosymbiosis influenced Margulis’s view of the world throughout her career. She was drawn to the connections between living things, and she realised that every creature lives in communities with many others. In 1991, she coined a word to describe this unity: holobiont, from the Greek for ‘whole unit of life’.22 It refers to a collection of organisms that spend significant parts of their lives together. The beewolf holobiont is the wasp plus all the bacteria in its antennae. The Ed Yong holobiont is me plus my bacteria, fungi, viruses, and more.
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Rosenberg pushed the holobiont concept into the world of genes. Evolutionary biologists had come to treat animals and other organisms as vehicles for their genes. The genes that create the best vehicles – say, the fastest cheetahs, or the hardiest corals, or the most resplendent birds of paradise – are more likely to be passed to the next generation. Over time, these genes become more common.
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evolution by natural selection depends on just three things: individuals must vary; those variations must be heritable; and those variations must have the potential to affect their fitness – that is, their ability to survive and reproduce. Variation, inheritance, fitness: if all three boxes are ticked, the engine of evolution whirrs into action, pumping out generations that are successively better adapted to their environment. An animal’s genes certainly meet this trinity of criteria.
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Rohwer feels that Rosenberg, by positioning the hologenome as the fundamental unit of selection, is glossing over those conflicts. Rosenberg seems to be saying that evolution acts to maximise the success of the whole – and that’s not what happens. It acts upon the parts as well, and those parts are often at odds.
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Diane Dodd showed that a fly’s diet could affect its sex life. She reared one strain of fruit flies on starch and another identical strain on maltose, a type of sugar. After 25 generations, the ‘starch flies’ preferred to mate with other starch flies, while the maltose flies were biased towards their own kind. It was a weird result. By changing the flies’ diet, Dodd had somehow altered their sexual preferences.
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"you hungry?"
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The Rosenbergs immediately said it had to be bacteria. An animal’s diet affects its microbiome; the microbes affect its smell; and its smell affects its attractiveness. It all made sense, and it fitted nicely with the hologenome concept. If they were right, the flies were evolving not just by changing their own genes, but by changing their microbes – just as the resistant Mediterranean corals had presumably done.
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If two groups of the same insect ignore each other and only mate within their social circles, they should eventually split into distinct species.
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Lynn Margulis echoed his views in 2002, claiming that the creation of new symbioses between distinct organisms – which she called symbiogenesis – has been the main force behind the origin of new species. To her, the kinds of relationships you’ve seen so far in this book were not just pillars of evolution, but its very foundations. She failed to make her case, though. She listed plenty of examples of symbiotic microbes that led to important evolutionary adaptations, but, crucially, presented almost no evidence that they actually gave rise to new species, much less that they are the principal ...more
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In 2001, Seth Bordenstein and his mentor Jack Werren were studying two closely related species of parasitic wasp: Nasonia giraulti and Nasonia longicornis. They have existed as separate species for just 400,000 years and to the untrained eye, they look identical – both tiny, with black bodies and orange legs. But they cannot breed. The two wasps carry different strains of Wolbachia; when they mate, the clash between these rival strains kills most of the hybrids. When Bordenstein took Wolbachia out of the equation with antibiotics, the hybrids survived. He showed that, in these wasps, ...more
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We’ve seen how individual animals rely on microbes for ordinary and essential aspects of their lives, like building organs or calibrating immune systems. We’ve also briefly seen that some microbes can bestow on their hosts more unusual abilities, from the illuminated camouflage of the bobtail squid to the regenerative skills of the Paracatenula flatworm. Now, we’ll see how other microbe-given superpowers have turned some groups of animals into evolutionary winners, which can digest indigestible foods, withstand inhospitable places, survive fatal meals, and otherwise succeed where other species ...more
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Slicing and dicing his way through innumerable species, he came to realise that symbiosis between animals and microbes was not a rare phenomenon, as others believed at the time. It was the rule rather than the exception: ‘a widespread, though always supplementary, device, enhancing the vital possibilities of the host animals in a multiplicity of ways’. His decades of work went into a magnum opus called Endosymbiosis of Animals with Plant Microorganisms
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What has Buchnera been doing for all of that time? Buchner had guessed the answer: he supposed that insect symbionts were mostly there for nutritional reasons, helping their hosts to digest their food. That’s certainly the case for many of the insects he studied, but for Buchnera the truth is slightly different. It doesn’t break down the aphid’s meals. It supplements them.
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Aphids feed on phloem sap – a sweet fluid that flows through plants. It is a superb food source in many ways: high in sugar, low in toxins, largely untapped by other animals. But it’s also woefully deficient in several nutrients, including ten essential amino acids that animals need to survive. A shortfall of any one of these would be devastating. A deficit of all ten is intolerable – unless something else can compensate. There is now overwhelming evidence that Buchnera is that something.
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For Riftia’s bacteria, that’s sulphur, or rather the sulphides that spew out of the vents. The bacteria oxidise these chemicals and use the liberated energy to fix carbon. This is chemosynthesis: making your own food using chemical energy instead of light or solar energy. And rather than producing oxygen as a waste product, as photosynthetic plants do, these chemosynthesising bacteria churn out pure sulphur. Hence the yellow crystals in Riftia’s trophosome.
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Chemosynthesis explains why the worms are gutless and mouthless: their symbionts provide them with all the food they need. Unlike aphids or sharpshooters, which rely on bacteria for amino acids, these worms rely on their symbionts for everything
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Dubilier found the answer in 2001, when she realised that they have two different symbionts: one big, one small, and both mingling beneath their skin.13 The small bacterium grabs sulphates, which are plentiful in Elba sediments, and converts them into sulphides. The big bacterium then oxidises the sulphides to power chemosynthesis, much like Riftia’s microbes. In the process, it produces sulphates that its smaller neighbour can reuse. The two microbes feed each other in a cycle of sulphur, which then feeds the worm – a symbiosis à trois. By adding the small sulphate-grabbing bacteria to their ...more
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Each sample she dried in an oven, pulped in a blender, and pulverised with a mortar and pestle. The smell was memorable. The reward was DNA, which allowed her to catalogue the microbes that lived in the guts of its maker.
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DNA and microbes
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Ley found that each mammal had its own distinctive set of gut microbes, but these communities clustered into certain groups depending on their owner’s ancestry and, in particular, their diet.14 The plant-eating herbivores typically had the highest diversity of bacteria. The meat-eating carnivores had the lowest. The omnivores, with their broad diets, were in the middle.
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Diet
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First, the explanation. Plants are by far the most abundant source of food on land, but it takes more enzymatic power to digest them. Compared to animal flesh, plant tissues contain more complex carbohydrates, such as cellulose, hemicellulose, lignin, and resistant starches. Vertebrates don’t have the molecular chops for breaking these apart. Bacteria do.
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The very first mammals were carnivores – small, scurrying, scourges of insects. Shifting from meat to plants was an evolutionary breakthrough for our group. The sheer abundance and variety of plants allowed herbivores to diversify much faster than their carnivore kin, and spread into niches that had been vacated by the demise of the large dinosaurs.
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mammalian success was founded on vegetarianism, and that vegetarianism was founded on microbes.
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Time and again, different groups of mammals swallowed plant-breaking microbes from their environments, and used their enzymes to mount assaults on leaves, shoots, stems, and twigs.
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Some foregut fermenters, like cattle, give their microbes even more time to work by ruminating – a distasteful but effective cycle of regurgitating, re-chewing and re-swallowing one’s stomach contents.
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The kangaroo is a hopping Australian marsupial and the okapi is a stripe-trousered giraffe-ish creature from Africa – but both are foregut fermenters and have broadly similar microbiomes. The pattern holds for hindgut fermenters as well.
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Fermenter
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In 1889, Joseph Leidy, an extraordinary American naturalist, cut open the guts of termites to find out what they were eating. As he watched the dissected insects under a microscope, he was shocked to see small specks fleeing from the corpses like ‘a multitude of persons from the door of a crowded meeting-house’. He billed them as ‘parasites’ but we now know that these tiny evacuees are protists: eukaryotic microbes that are more complex than bacteria but still consist of a single cell. The protists can make up half the weight of their termite host, and they are abundant for a reason: they have ...more
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Termites
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Inside their cavernous nests, they farm a fungus, which they feed with bits of wooden shrapnel. The fungus splits cellulose into smaller components, creating a compost that the termites then eat. Inside their guts, bacteria digest the fragments even further. The termites themselves contribute very little to this assault; their main role is to harbour the bacteria and cultivate the fungus. Without either partner, they starve.
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Fungus and bacteria
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A macrotermite queen takes things even further. She is enormous. Her torso is the length of a fingernail but her abdomen is a palm-sized, pulsating, egg-laying sac, so grossly distended that she cannot move. She also has a distinct lack of gut microbes. Instead, she relies on her worker daughters (and their microbes) to feed her. Her entire colony – thousands of workers, billions of microbes, and giant nests laced with wood-breaking fungus – functions as her gut.
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And with each new meal or mouthful, we select for microbes that are best at digesting whatever we’ve just eaten. They react with incredible speed. One study asked ten volunteers to stick to two strict diets for five days each: one rich in fruit, vegetables, and grains, and the other heavy in meat, eggs, and cheese. 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.25 In fact, these two kinds of community looked a lot like the gut microbes of ...more
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interesting. the switching between microbes
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As a general rule, organisms don’t line up to be consumed. They defend themselves. Animals have the option to fight or flee, but plants, being more passive, rely more on chemical defences. They fill their tissues with substances that deter plant-eaters – poisons that harm, sterilise, cause weight loss, initiate tumours, trigger abortions, lead to neurological disorders, and just plain kill.
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Animals have many ways of getting around plant poisons, but each solution has a cost. They could eat the least toxic parts, but fussiness restricts opportunities. They could swallow neutralising substances like clay, but antidotes take time and effort to find. They could make their own detoxifying enzymes, but that takes energy. Bacteria offer an alternative. They are masters of biochemistry, and can degrade everything from heavy metals to crude oil.
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He took the faecal pellets of the experienced rodents, pulped them in a blender, and fed them to the naïve ones to give them an infusion of detoxifying microbes. Suddenly, these individuals could happily eat creosote.
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Interesting
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With each mouthful, it takes in microbes that live on the surface of the creosote; perhaps these have already evolved ways of breaking down the resin cocktail. Having eaten these microbes, the rat is itself better equipped. Later, it scurries away and defecates, leaving a small microbe-filled pellet behind – which another woodrat finds and eats. The ability spreads. Eventually, the rats unlocked the ability to eat what would soon become the most common plant in the Mojave.
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If you want to defend yourself from another creature or eat a new source of food, there’s almost certainly a microbe that already has the right tools for the job. And if there isn’t, there soon will be: these things reproduce rapidly and swap genes readily.
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And they had established J-liv as a probiotic: a term that is most commonly linked to yoghurts and supplements, but really applies to any microbe that can be applied to a host to improve its health.
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J-liv. Yoghurts and supplements
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Science has certainly tried.15 In the 1930s, Japanese microbiologist Minoru Shirota led the quest by looking for hardy microbes that could reach the gut without first being destroyed by the stomach’s acids. He eventually homed in on a strain of Lactobacillus casei, grew it in fermented milk, and, in 1935, created the first bottle of the dairy drink called Yakult. Today, the company sells around 12 billion bottles a year, worldwide. Overall, the probiotics industry is a multi-billion-dollar business. Its products feed our stomachs along with our desire for ‘natural’ healthcare (even though many ...more
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yakult
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Gulping down a yoghurt is like ingesting scarcity. Rarity, too: the bacteria in these products are not important members of the adult gut. They largely belong to the same category that Metchnikoff canonised – makers of lactic acid, like Lactobacillus and Bifidobacterium, which were chosen more for practical reasons than scientific ones. They are easy to grow, they are already found in fermented foods, and they can survive the trip through both a commercial packaging plant and a consumer’s stomach. ‘But most of them never arose in the human gut, and they don’t have the factors that allow them ...more
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activia
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Some would argue that this doesn’t matter – the breeze can still rattle objects along its path. Gordon’s team saw some signs of this: the yoghurt they studied could nudge the microbes in mouse guts into activating genes for digesting carbohydrates, albeit temporarily. Wendy Garrett later found that a strain of Lactococcus lactis can help mice without sticking around – or even staying alive.
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can help without sticking around or even staying alive
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When it enters a mouse’s guts it bursts apart, and in its death it releases enzymes that can reduce inflammation. It might be a poor coloniser, but it can still do some good.
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yoghurt
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the Cochrane Collaboration – a respected non-profit organisation that methodically reviews medical studies – has done exactly that. According to their verdicts, probiotics can shorten bouts of infectious diarrhoea, and reduce the risk of diarrhoea brought about by antibiotic treatments. They can also save lives from necrotising enterocolitis – a horrible gut disease that affects premature infants. And there ends the list. Compared to the hype, it’s modest. There is still no clear evidence that probiotics help people with allergies, asthma, eczema, obesity, diabetes, more common types of IBD, ...more
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