I Contain Multitudes
DEDICATION
For Mum
CONTENTS
Dedication
Prologue: A Trip to the Zoo
1. Living Islands
2. The People Who Thought to Look
3. Body Builders
4. Terms and Conditions Apply
5. In Sickness and in Health
6. The Long Waltz
7. Mutually Assured Success
8. Allegro in E Major
9. Microbes à la Carte
10. Tomorrow the World
Acknowledgements
List of Illustrations
Notes
Bibliography
Index
Photos Section
About the Author
Credits
Copyright
About the Publisher
PROLOGUE: A TRIP TO THE ZOO
Baba does not flinch. He is unfazed by the throng of excited kids who have gathered around him. He is unperturbed by the Californian summer heat. He does not mind the cotton swabs that brush his face, body and paws. His nonchalance makes sense, for his life is safe and cushy. He lives in San Diego Zoo, wears an impregnable suit of armour, and is currently curled around the waist of a zookeeper. Baba is a white-bellied pangolin – an utterly endearing animal that looks like a cross between an anteater and a pine cone. He’s about the size of a small cat. His black eyes have a doleful air, and the hair that frames his cheeks look like unruly mutton chops. His pink face ends in a tapering toothless snout that’s well adapted for slurping up ants and termites. His stocky front legs are tipped with long, curved claws for clinging to tree trunks and tearing into insect nests, and he has a long tail for hanging off tree branches (or friendly zookeepers).
But his most distinctive features, by far, are his scales. His head, body, limbs and tail are covered in them – pale orange, overlapping plates that create an extremely tough defensive coat. They are made of the same material as your nails – keratin. Indeed, they look and feel a lot like fingernails, albeit large, varnished, and badly chewed ones. Each one is flexibly but firmly attached to his body, so they sink down and spring back as I run my hand down his back. If I stroked him in the opposite direction, I’d probably cut myself – many of the scales are sharp-edged. Only Baba’s face, belly and paws are unprotected, and if he chose to, he could easily defend them by rolling up into a ball. It’s this ability that gives his kind their name: pangolin comes from the Malay word “pengguling”, meaning “something that rolls up”.
Baba is one of the zoo’s ambassador animals – exceptionally docile and well-trained individuals who take part in public activities. Keepers frequently take him to nursing homes and children’s hospitals to brighten up the days of sick people, and to teach them about unusual animals. But today, he gets the day off. He just sits around the keeper’s midriff, like the world’s strangest cummerbund, while Rob Knight gently dabs a cotton swab against the side of his face. “This is one of the species that I’ve been captivated by since I was a kid – just that something like that exists,” he says.
Knight, a tall, lanky New Zealander with buzzcut hair, is a scholar of microscopic life, a connoisseur of the invisible. He studies bacteria and other microscopic organisms – microbes – and he is specifically enthralled by those that live in or on the bodies of animals. To study them, he must first collect them. Butterfly collectors use nets and jars; Knight’s tool of choice is the cotton swab. He reaches over with a small bud and rolls it over Baba’s nose for a couple of seconds, long enough to infuse the end with pangolin bacteria. Thousands, if not millions, of microscopic cells are now entangled in the white fuzz. Knight moves delicately so as not to perturb the pangolin. Baba couldn’t look less perturbed if he tried. I get the feeling that if a bomb went off next to him/his only reaction would be to fidget slightly.
Baba is not just a pangolin. He is also a teeming mass of microbes. Some of them live inside him, mostly in his gut. Others live on the surface, on his face, belly, paws, claws, and scales. Knight swabs each of these places in turn. He has swabbed his own body parts on more than one occasion, for he too hosts his own community of microbes. So do I. So does every beast in the zoo. So does every creature on the planet, except for a few lab animals that scientists have deliberately bred to be sterile.
All of us have an abundant microscopic menagerie, collectively known as the microbiota or microbiome.1 They live on our surface, inside our bodies, and sometimes inside our very cells. The vast majority of them are bacteria, but there are also other tiny organisms including fungi (such as yeasts) and archaea, a mysterious group that we will meet again later. There are viruses too, in unfathomable numbers – a “virome” that infects all the other microbes and occasionally the host’s cells. We can’t see any of these minuscule specks. But if our own cells were to mysteriously disappear, they would perhaps be detectable as a ghostly microbial shimmer, outlining a now-vanished animal core.2
In some cases, the missing cells would barely be noticeable. Sponges are among the simplest of animals, with static bodies never more than a few cells thick, and they are also home to a thriving microbiome.3 Sometimes, if you look at a sponge under a microscope, you will barely be able to see the animal for the microbes that cover it. The even simpler placozoans are little more than oozing mats of cells; they look like amoebae but they are animals like us, and they also have microbial partners. Ants live in colonies that can number in their millions, but every single ant is a colony unto itself. A polar bear, trundling solo through the Arctic, with nothing but ice in all directions, is completely surrounded. Bar-headed geese carry microbes over the Himalayas, while elephant seals take them into the deepest oceans. When Neil Armstrong and Buzz Aldrin set foot on the Moon, they were also taking giant steps for microbe-kind.
When Orson Welles said “We’re born alone, we live alone, we die alone”, he was mistaken. Even when we are alone, we are never alone. We exist in symbiosis – a wonderful term that refers to different organisms living together. Some animals are colonised by microbes while they are still unfertilised eggs; others pick up their first partners at the moment of birth. We then proceed through our lives in their presence. When we eat, so do they. When we travel, they come along. When we die, they consume us. Every one of us is a zoo in our own right – a colony enclosed within a single body. A multi-species collective. An entire world.
These concepts can be hard to grasp, not least because we humans are a global species. Our reach is boundless. We have expanded into every corner of our blue marble, and some of us have even left it. It can be weird to consider existences that play out in an intestine or in a single cell, or to think about our body parts as rolling landscapes. And yet, they assuredly are. The Earth contains a variety of different ecosystems: rainforests, grasslands, coral reefs, deserts, salt marshes, each with its own particular community of species. But a single animal is full of ecosystems too. Skin, mouth, guts, genitals, any organ that connects with the outside world: each has its own characteristic community of microbes.4 All of the concepts that ecologists use to describe the continental-scale ecosystems that we see through satellites also apply to ecosystems in our bodies that we peer at with microscopes. We can talk about the diversity of microbial species. We can draw food webs, where different organisms eat and feed each other. We can single out keystone microbes that exert a disproportionate influence on their environment – the equivalents of sea otters or wolves. We can treat disease-causing microbes – pathogens – as invasive creatures, like cane toads or fire ants. We can compare the gut of a person with inflammatory bowel disease to a dying coral reef or a fallow field: a battered ecosystem where the balance of organisms has gone awry.
These similarities mean that when we look at
a termite or a sponge or a mouse, we are also looking at ourselves. Their microbes might be different to ours, but the same principles govern our alliances. A squid with luminous bacteria that glow only at night can tell us about the daily ebbs and flows of bacteria in our guts. A coral reef whose microbes are running amok because of pollution or overfishing hints at the turmoil that occurs in our guts when we swallow unhealthy food or antibiotics. A mouse whose behaviour changes under the sway of its gut microbes can show us something about the tendrils of influence that our own companions insinuate into our minds. Through microbes, we find unity with our fellow creatures, despite our incredibly different lives. None of those lives is lived in isolation; they always exist in a microbial context, and involve constant negotiations between species big and small. Microbes move between animals, too, and between our bodies and the soils, water, air, buildings, and other environments around us. They connect us to each other, and to the world.
All zoology is really ecology. We cannot fully understand the lives of animals without understanding our microbes and our symbioses with them. And we cannot fully appreciate our own microbiome without appreciating how those of our fellow species enrich and influence their lives. We need to zoom out to the entire animal kingdom, while zooming in to see the hidden ecosystems that exist in every creature. When we look at beetles and elephants, sea urchins and earthworms, parents and friends, we see individuals, working their way through life as a bunch of cells in a single body, driven by a single brain, and operating with a single genome. This is a pleasant fiction. 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.”5
1. LIVING ISLANDS
The Earth is 4.54 billion years old. A span of time that big is too mind-boggling to comprehend, so let’s collapse the planet’s entire history into a single calendar year.1 Right now, as you’re reading this page, it is 31st December, just before the stroke of midnight. (Thankfully, fireworks were invented nine seconds ago.) Humans have only existed for the 30 minutes or fewer. The dinosaurs ruled the world until the evening of 26th December, when an asteroid hit the planet and wiped them out (except for the birds). Flowers and mammals evolved earlier in December. In November, plants invaded the land and most of the major animal groups appeared in the seas. Plants and animals are all made up of many cells, and similar multicellular organisms had certainly evolved by the start of October. They may have appeared before that – the fossils are ambiguous and open to interpretation – but they would have been rare. Before October, almost every living thing on the planet consisted of single cells. They would have been invisible to the naked eye, had eyes existed. They had been that way ever since life first emerged, some time in March.
Let me stress: all the visible organisms that we’re familiar with, everything that springs to mind when we think of “nature”, are latecomers to life’s story. They are part of the coda. For most of the tale, microbes were the only living things on Earth. From March to October in our imaginary calendar, they had the sole run of the planet.
During that time, they changed it irrevocably. Bacteria enrich soils and break down pollutants. They drive planetary cycles of carbon, nitrogen, sulphur and phosphorus, by converting these elements into compounds that can be used by animals and plants and then returning them to the world by decomposing organic bodies. They were the first organisms to make their own food, by harnessing the sun’s energy in a process called photosynthesis. They released oxygen as a waste product, pumping out so much of the gas that they permanently changed the atmosphere of our planet. It is thanks to them that we live in an oxygenated world. Even now, the photosynthetic bacteria in the oceans produce the oxygen in half the breaths you take, and they lock away an equal amount of carbon dioxide.2 It is said that we are now in the Anthropocene: a new geological period characterised by the enormous impact that humans have had on the planet. You could equally argue that we are still living in the Microbiocene: a period that started at the dawn of life itself and will continue to its very end.
Indeed, microbes are everywhere. They live in the water of the deepest oceanic trenches and in the rocks below. They persist in belching hydrothermal vents, boiling springs, and Antarctic ice. They can even be found in clouds, where they act as seeds for rain and snow. They exist in astronomical numbers. Actually, they far exceed astronomical numbers: there are more bacteria in your gut than there are stars in our galaxy.3
This is the world in which animals originated, one smothered in and transformed by microbes. As palaeontologist Andrew Knoll once said, “Animals might be evolution’s icing, but bacteria are really the cake.”4 They have always been part of our ecology. We evolved among them. Also, we evolved from them. Animals belong to a group of organisms called eukaryotes, which also includes every plant, fungus and alga. Despite our obvious variety, all eukaryotes are built from cells that share the same basic architecture, which distinguishes them from other forms of life. They pack almost all their DNA into a central nucleus, a structure that gives the group its name – “eukaryote” comes from the Greek for “true nut”. They have an internal “skeleton” that provides structural support and shuttles molecules from place to place. And they have mitochondria – bean-shaped power stations that supply cells with energy.
All eukaryotes share these traits because we all evolved from a single ancestor, around two billion years ago. Before that point, life on Earth could be divided into two camps or domains: the bacteria, which we already know about, and the archaea, which are less familiar and have a fondness for colonising inhospitable and extreme environments. These two groups both consisted of single cells that lack the sophistication of eukaryotes. They had no internal skeleton. They lacked a nucleus. They had no energy-providing mitochondria, for reasons that will soon become abundantly clear. They also looked superficially similar, which is why scientists originally believed that archaea were bacteria. But appearances are deceptive; archaea are as different from bacteria in biochemistry as PCs are from Macs in operating systems.
For roughly the first 2.5 billion years of life on Earth, bacteria and archaea charted largely separate evolutionary courses. Then, on one fateful occasion, a bacterium somehow merged with an archaeon, losing its free-living existence and becoming entrapped forever within its new host. That is how many scientists believe eukaryotes came to be. It’s our creation story: two great domains of life merging to create a third, in the greatest symbiosis of all time. The archaeon provided the chassis of the eukaryotic cell while the bacterium eventually transformed into the mitochondria.5
All eukaryotes descend from that fateful union. It’s why our genomes contain many genes that still have an archaeal character and others that more resemble those of bacteria. It’s also is why all of us contain mitochondria in our cells. These domesticated bacteria changed everything. By providing an extra source of energy, they allowed eukaryotic cells to get bigger, to accumulate more genes, and to become more complex. This explains what biochemist Nick Lane calls the “black hole at the heart of biology”. There’s a huge void between the simpler cells of bacteria and archaea and the more complex ones of eukaryotes, and life has managed to cross that void exactly once in four billion years. Since then, the countless bacteria and archaea in the world, all evolving at breakneck speed, have never again managed to produce a eukaryote. How could that possibly be? Other complex structures, from eyes to armour to many-celled bodies, have evolved on many independent occasions but the eukaryotic cell is a one-off innovation. That’s because, as Lane and others argue, the merger that created it – the one between an archaeon and a bacterium – was so breathtakingly improbable that it has never been duplicated, or at least never with success. By forging a union, those two microbes defied the odds and enabled the existence of all plants, animals, and anything visible to the naked eye – or anything with eyes, for that matter. They’re the reason I exist to write this book and you exist to read
it. In our imaginary calendar, their merger happened some time in the middle of July. This book is about what happened afterwards.
After eukaryotic cells evolved, some of them started cooperating and clustering together, giving rise to multicellular creatures, like animals and plants. For the first time, living things became big – so big that they could host huge communities of bacteria and other microbes in their bodies.6 Counting such microbes is difficult. It’s commonly said that the average person contains ten microbial cells for every human one, making us rounding errors in our own bodies. But this 10-to-1 ratio, which shows up in books, magazines, TED talks, and virtually every scientific review on this topic, is a wild guess, based on a back-of-the-envelope calculation that became unfortunately enshrined as fact.7 The latest estimates suggest that we have around 30 trillion human cells and 39 trillion microbial ones – a roughly even split. Even these numbers are inexact, but that does not really matter: by any reckoning, we contain multitudes.
If we zoomed in on our skin, we would see them: spherical beads, sausage-like rods, and comma-shaped beans, each just a few millionths of a metre across. They are so small that, despite their numbers, they collectively weigh just a few pounds in total. A dozen or more would line up cosily in the width of a human hair. A million could dance on the head of a pin.
Without access to a microscope, most of us will never directly glimpse these miniature organisms. We only notice their consequences, and especially the negative ones. We can feel the painful cramp of an inflamed gut, and hear the sound of an uncontrollable sneeze. We can’t see the bacterium Mycobacterium tuberculosis with our naked eyes, but we can see the bloody spittle of a tuberculosis patient. Yersinia pestis, another bacterium, is similarly invisible to us, but the plague epidemics that it causes are all too obvious. These disease-causing microbes – pathogens – have traumatised humans throughout history, and have left a lingering cultural scar. Most of us still see microbes as germs: unwanted bringers of pestilence that we must avoid at all costs. Newspapers regularly churn out scare stories in which everyday items, from keyboards to mobile phones to doorknobs, turn out to be – gasp! – covered in bacteria. Even more bacteria than on a toilet seat! The implication is that these microbes are contaminants, and their presence a sign of filth, squalor, and imminent disease. This stereotype is grossly unfair. Most microbes are not pathogens. They do not make us sick. There are fewer than 100 species of bacteria that cause infectious diseases in humans;8 by contrast, the thousands of species in our guts are mostly harmless. At worst, they are passengers or hitchhikers. At best, they are invaluable parts of our bodies: not takers of life but its guardians. They behave like a hidden organ, as important as a stomach or an eye but made of trillions of swarming individual cells rather than a single unified mass.