I Contain Multitudes Read online

  The microbiome is infinitely more versatile than any of our familiar body parts. Your cells carry between 20,000 and 25,000 genes, but it is estimated that the microbes inside you wield around 500 times more.9 This genetic wealth, combined with their rapid evolution, makes them virtuosos of biochemistry, able to adapt to any possible challenge. They help to digest our food, releasing otherwise inaccessible nutrients. They produce vitamins and minerals that are missing from our diet. They break down toxins and hazardous chemicals. They protect us from disease by crowding out more dangerous microbes or killing them directly with antimicrobial chemicals. They produce substances that affect the way we smell. They are such an inevitable presence that we have outsourced surprising aspects of our lives to them. They guide the construction of our bodies, releasing molecules and signals that steer the growth of our organs. They educate our immune system, teaching it to tell friend from foe. They affect the development of the nervous system, and perhaps even influence our behaviour. They contribute to our lives in profound and wide-ranging ways; no corner of our biology is untouched. If we ignore them, we are looking at our lives through a keyhole.

  This book will open the door fully. We are going to explore the incredible universe that exists within our bodies. We’ll learn about the origins of our alliances with microbes, the counter-intuitive ways in which they sculpt our bodies and shape our everyday lives, and the tricks we use for keeping them in line and ensuring a cordial partnership. We’ll look at how we inadvertently disrupt these partnerships and, in doing so, jeopardise our health. We’ll see how we might reverse these problems by manipulating the microbiome for our benefit. And we’ll hear the stories of the gleeful, imaginative, driven scientists who have dedicated their lives to understanding the microbial world, often in the face of scorn, dismissal, and failure.

  We won’t focus only on humans, either.10 We’ll see how microbes have bestowed on animals extraordinary powers, evolutionary opportunities, and even their own genes. The hoopoe, a bird with a pickaxe profile and a tiger’s colours, paints its eggs with a bacteria-rich fluid that it secretes from a gland beneath its tail; the bacteria release antibiotics that stop more dangerous microbes from infiltrating the eggs and harming the chicks. Leafcutter ants also carry antibiotic-producing microbes on their bodies, and use these to disinfect the fungi that they cultivate in underground gardens. The spiky, expandable pufferfish uses bacteria to make tetrodotoxin – an exceptionally lethal substance which poisons any predator that tries to eat it. The Colorado potato beetle, a major pest, uses bacteria in its saliva to suppress the defences of the plants that it eats. The zebra-striped cardinalfish houses luminous bacteria, which it uses to attract its prey. The ant lion, a predatory insect with fearsome jaws, paralyses its victims with toxins produced by the bacteria in its saliva. Some nematode worms kill insects by vomiting toxic glowing bacteria into their bodies;11 others burrow into plant cells, and cause vast agricultural losses, using genes stolen from microbes.

  Our alliances with microbes have repeatedly changed the course of animal evolution and transformed the world around us. It is easiest to appreciate how important these partnerships are by considering what would happen if they broke. Imagine if all microbes on the planet suddenly disappeared. On the upside, infectious diseases would be a thing of the past, and many pest insects would be unable to eke out a living. But that’s where the good news ends. Grazing mammals, like cows, sheep, antelope, and deer would starve since they are utterly dependent on their gut microbes to break down the tough fibres in the plants they eat. The great herds of Africa’s grasslands would vanish. Termites are similarly dependent on the digestive services of microbes, so they would also disappear, as would the larger animals that depend on them for food, or on their mounds for shelter. Aphids, cicadas, and other sap-sucking bugs would perish without bacteria to supplement the nutrients that are missing from their diets. In the deep oceans, many worms, shellfish, and other animals rely on bacteria for all of their energy. Without microbes, they too would die, and the entire food webs of these dark, abyssal worlds would collapse. Shallower oceans would fare little better. Corals, which depend on microscopic algae and a surprisingly diverse collection of bacteria, would become weak and vulnerable. Their mighty reefs would bleach and erode, and all the life they support would suffer.

  Humans, oddly, would be fine. Unlike other animals, for whom sterility would mean a quick death, we would get by for weeks, months, even years. Our health might eventually suffer, but we’d have more pressing concerns. Waste would rapidly build up, for microbes are lords of decay. Along with other grazing mammals, our livestock would perish. So would our crop plants; without microbes to provide plants with nitrogen, the Earth would experience a catastrophic de-greening. (Since this book focuses entirely on animals, I offer my sincerest apologies to enthusiasts of botany.) “We predict complete societal collapse only within a year or so, linked to catastrophic failure of the food supply chain,” wrote microbiologists Jack Gilbert and Josh Neufeld, after running through this thought experiment.12 “Most species on Earth would become extinct, and population sizes would be reduced greatly for the species that endured.”

  Microbes matter. We have ignored them. We have feared and hated them. Now, it is time to appreciate them, for our grasp of our own biology is greatly impoverished if we don’t. In this book, I want to show you what the animal kingdom really looks like, and how much more wondrous it becomes when you see it as the world of partnerships that it actually is. This is a version of natural history that deepens the more familiar one, the one laid down by the greatest naturalists of the past.

  In March 1854, a 31-year-old British man named Alfred Russel Wallace began an epic eight-year trek through the islands of Malaysia and Indonesia.13 He saw fiery-furred orang-utans, kangaroos that hopped in trees, resplendent birds of paradise, giant birdwing butterflies, the babirusa pig whose tusks grow up through its snout, and a frog that glides from tree to tree on parachute-like feet. Wallace netted, grabbed, and shot the wonders he saw, eventually amassing an astonishing collection of over 125,000 specimens: shells; plants; thousands of insects, pinned in trays; birds and mammals, skinned, stuffed, or preserved in spirits. But unlike many of his contemporaries, Wallace also labelled everything meticulously, noting where each specimen was collected.

  That was crucial. From these details, Wallace extracted patterns. He noticed a lot of variation in the animals that live in a certain place, even among those of the same species. He saw that some islands were home to unique species. He realised that as he sailed east from Bali to Lombok – a distance of just 22 miles – the animals of Asia suddenly gave way to the very different fauna of Australasia, as if these two islands were separated by an invisible barrier (which would later be called the Wallace Line). For good reason, Wallace is today heralded as the father of biogeography – the science of where species are, and where they are not. But as David Quammen writes in The Song of the Dodo: “As practiced by thoughtful scientists, biogeography does more than ask Which species? and Where? It also asks Why? And, what is sometimes even more crucial, Why not?”14

  The study of microbiomes begins in exactly this way: cataloguing the ones that are found on different animals, or on different body parts of the same animal. Which species live where? Why? And why not? We need to know their biogeography before we can gain deeper insights into their contributions. Wallace’s observations and specimens led him towards the defining insight of biology: that species change. “Every species has come into existence coincident both in space and time with a pre-existing closely allied species,” he wrote, repeatedly and sometimes in italics.15 As animals compete, the fittest individuals survive and reproduce, passing their advantageous traits to their offspring. That is, they evolve, by means of natural selection. This was as important an epiphany as science has ever produced, and it all began with a restless curiosity about the world, a desire to explore it, and an aptitude for noticing what lives where.

  Wallace was
just one of many naturalist explorers who traipsed around the world and catalogued its riches. Charles Darwin endured a five-year, round-the-world voyage aboard the HMS Beagle, in which he would discover the fossilised bones of giant ground sloths and armadillos in Argentina, and encounter the giant tortoises, marine iguanas, and diverse mockingbirds of the Galapagos Islands. His experiences and collections planted the intellectual seeds of the same idea that had independently germinated in Wallace’s mind – the theory of evolution, which would become inextricably linked with his name. Thomas Henry Huxley, who became known as ‘Darwin’s bulldog’ for his ferocious advocacy of natural selection, sailed to Australia and New Guinea and studied their marine invertebrates. The botanist Joseph Hooker meandered his way to Antarctica, collecting plants along the way. More recently, E. O. Wilson, after studying the ants of Melanesia, wrote the textbook on biogeography.

  It is often assumed that these legendary scientists focused entirely on the visible worlds of animals and plants, ignoring the hidden worlds of microbes. That is not entirely true. Darwin certainly collected microbes – he called them “infusoria” – that blew onto the deck of the Beagle, and he corresponded with the leading microbiologists of the day.16 But there was only so much he could do with the tools available to him.

  By contrast, today’s scientists can collect samples of microbes, break them apart, extract their DNA, and identify them by sequencing their genes. In this way, they can do exactly what Darwin and Wallace did. They can collect specimens from different locations, identify them, and ask the fundamental question: what lives where? They can do biogeography – just on a different scale. The gentle caress of a cotton bud replaces the swing of a butterfly net. A read-out of genes is like a flick through a field guide. And an afternoon at the zoo, walking from cage to cage, can be like the voyage of the Beagle, sailing from island to island.

  Darwin, Wallace and their peers were particularly fascinated by islands, and for good reason. Islands are where you go if you want to find life at its most outlandish, gaudy, and superlative. Their isolation, restricted boundaries, and constrained size allow evolution to go to town. The patterns of biology resolve into sharper focus more readily than they would do on the extensive, contiguous mainland. But an island doesn’t have to be a land mass surrounded by water. To microbes, every host is effectively an island – a world surrounded by void. My hand, reaching out and stroking Baba at San Diego Zoo, is like a raft, conveying species from a human-shaped island to a pangolin-shaped one. An adult being ravaged by cholera is like Guam being invaded by foreign snakes. No man is an island? Not so: we’re all islands from a bacterium’s point of view.17

  Each of us has our own distinctive microbiome, sculpted by the genes we inherited, the places we’ve lived in, the drugs we’ve taken, the food we’ve eaten, the years we’ve lived, the hands we’ve shaken. Microbially, we are similar but different. When microbiologists first started cataloguing the human microbiome in its entirety they hoped to discover a “core” microbiome: a group of species that everyone shares. It’s now debatable if that core exists.18 Some species are common, but none is everywhere. If there is a core, it exists at the level of functions, not organisms. There are certain jobs, like digesting a certain nutrient or carrying out a specific metabolic trick, that are always filled by some microbe – just not always the same one. You see the same trend on a bigger scale. In New Zealand, kiwis root through leaf litter in search of worms, doing what a badger might do in England. Tigers and clouded leopards stalk the forests of Sumatra but in cat-free Madagascar that same niche is filled by a giant killer mongoose called the fossa; meanwhile, in Komodo, a huge lizard claims the top predator role. Different islands, different species, same jobs. The islands in question could be huge land masses, or individual people.

  In fact, every individual is more like an archipelago – a chain of islands. Each of our body parts has its own microbial fauna, just as the various Galapagos islands have their own special tortoises and finches. The human skin microbiome is the domain of Propionibacterium, Corynebacterium, and Staphylococcus, while Bacteroides lords over the gut, Lactobacillus dominates the vagina, and Streptococcus rules the mouth. Every organ is also variable in itself. The microbes that live at the start of the small intestine are very different from those in the rectum. Those in dental plaque vary above and below the gum-line. On the skin, microbes in the oily lakes of the face and chest differ from those in the hot and humid jungles of the groin and armpit, or those colonising the dry deserts of the forearms and palms. Speaking of palms, your right hand shares just a sixth of its microbial species with your left hand.19 The variations that exist between body parts dwarf those that exist between people. Put simply, the bacteria on your forearm are more similar to those on my forearm than to those in your mouth.

  The microbiome varies in time as well as space. When each baby is born, it leaves the sterile world of its mother’s womb and is immediately colonised by her vaginal microbes; almost three-quarters of a newborn’s strains can be traced directly back to its mother. Then follows an age of expansion. As the baby picks up new species from its parents and environment, its gut microbiome becomes gradually more diverse.20 The dominant species rise and fall: as the baby’s diet changes, milk-digesting specialists like Bifidobacterium give way to carbohydrate-eaters like Bacteroides. And as the microbes change, so do their antics. They start making different vitamins and they unlock the ability to digest a more adult diet.

  This period is turbulent but follows predictable stages. Imagine watching a forest recently scoured by fire, or a fresh island newly risen from the sea. Both would quickly be colonised by simple plants like lichens and mosses. Grasses and small shrubs would follow. Taller trees would arrive later. Ecologists call this succession, and it applies to microbes too. It takes anywhere from one to three years for a baby’s microbiome to reach an adult state. Then, a lasting stability. The microbiome may vary from day to day, from sunrise to sunset, or even from meal to meal, but such variations are small compared to the early changes. This dynamism of the adult microbiome conceals a background of constancy.21

  The exact pattern of succession will vary between different animals, because we turn out to be picky hosts. We are not just colonised by whatever microbes happen to land on us. We also have ways of selecting their microbial partners. We’ll learn about these tricks, but for now let us simply note that the human microbiome is distinct from the chimpanzee microbiome, which looks different from the gorilla microbiome, just as the forests of Borneo (orang-utans, pygmy elephants, gibbons) are distinct from those in Madagascar (lemurs, fossas, chameleons) or New Guinea (birds of paradise, tree kangaroos, cassowaries). We know this because scientists have swabbed and sequenced their way around the entire animal kingdom. They have described the microbiomes of pandas, wallabies, Komodo dragons, dolphins, lorises, earthworms, leeches, bumblebees, cicadas, tube worms, aphids, polar bears, dugongs, pythons, alligators, tsetse flies, penguins, kakapos, oysters, capybaras, vampire bats, marine iguanas, cuckoos, turkeys, turkey vultures, baboons, stick insects, and so many more. They have sequenced the microbiomes of human infants, premature babies, children, adults, the elderly, pregnant women, twins, city dwellers from the USA or China, rural villagers from Burkina Faso or Malawi, hunter-gatherers from Cameroon or Tanzania, Amazonian people who had never been contacted before, lean and fat people, and those in perfect health versus those with disease.

  These kinds of studies have blossomed. Even though the science of the microbiome is actually centuries old, it has picked up tremendous pace in the last few decades, thanks to technological improvements and the dawning realisation that microbes matter enormously to us – especially in a medical setting. They affect our bodies so extensively that they can determine how well we respond to vaccines, how much nourishment children can extract from their food, and how well cancer patients respond to their drugs. Many conditions, including obesity, asthma, colon cancer, diabetes, and autism, are accompanied by change
s in the microbiome, suggesting that these microbes are at the very least a sign of illness, and at most a cause of it. If it’s the latter, we might be able to substantially improve our health by tweaking our microbial communities: by adding and subtracting species, transplanting entire communities from one person to another, and engineering synthetic organisms. We can even manipulate the microbiomes of other animals, breaking partnerships that allow parasitic worms to afflict us with horrendous tropical diseases, while forging new symbioses that allow mosquitoes to fight off the virus behind dengue fever.

  This is a rapidly changing field of science, and one still shrouded in uncertainty, inscrutability, and controversy. We cannot even identify many of the microbes in our bodies, let alone work out how they affect our lives or our health. But that is exciting! It is surely better to be on the crest of a wave, looking at the ride ahead, than to have already washed up on shore. Hundreds of scientists are now surfing that wave. Funds are flowing in. The number of relevant scientific papers has risen exponentially. Microbes have always ruled the planet but for the first time in history, they are fashionable. “This was completely backwater science; now it’s front-seat science,” says biologist Margaret McFall-Ngai. “It’s been fun to watch people realising that microbes are the centre of the universe, and to see the field blossom. We now know that they make up the vast diversity of the biosphere, that they live in intimate association with animals, and that animal biology was shaped by interacting with microbes. In my mind, this is the most significant revolution in biology since Darwin.”