I Contain Multitudes: The Microbes Within Us and a Grander View of Life

by Ed Yong

Baba is a white-bellied pangolin – an utterly endearing animal that looks like a cross between an anteater and a pine cone.

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.

The ant lion, a predatory insect with fearsome jaws, paralyses its victims with toxins produced by the bacteria in its saliva.

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.

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.

our microbes control the storage of fat and the creation of new blood vessels, and that obese individuals have different gut microbes to lean ones.

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.

Biologists speak of a ‘gut–brain axis’ – a two-way line of communication between the gut and the brain. We now know that gut microbes are part of this axis, in both directions.

All of this means that labels like mutualist, commensal, pathogen, or parasite don’t quite work as badges of fixed identity. These terms are more like states of being, like hungry or awake or alive, or behaviours like cooperating or fighting. They’re adjectives and verbs rather than nouns: they describe how two partners relate to one another at a given time and place.

Even symbionts as essential and long-standing as mitochondria, the energy-providing power plants that exist in all animals’ cells, can wreak havoc if they end up in the wrong place. A cut or a bruise can split some of your cells apart and spill fragments of mitochondria into your blood – fragments that still keep some of their ancient bacterial character. When your immune system spots them, it mistakenly assumes that an infection is under way and mounts a strong defence. If the injury is severe, and enough mitochondria are released, the resulting body-wide inflammation can build into a lethal condition called systemic inflammatory response syndrome (SIRS).

Couples might work well together, but if one partner can get the same benefits without spending as much energy or effort, it will do so unless punished or policed.

H. G. Wells wrote about this in 1930: ‘Every symbiosis is, in its degree, underlain with hostility, and only by proper regulation and often elaborate adjustment can the state of mutual benefit be maintained. Even in human affairs, the partnerships for mutual benefit are not so easily kept up, in spite of me being endowed with intelligence and so being able to grasp the meaning of such a relation. But in lower organisms, there is no such comprehension to help keep the relationship going. Mutual partnerships are adaptations as blindly entered into and as unconsciously brought about as any others.’13

To many scientists, however, warding off pathogens is just a bonus trick. The immune system’s main function is to manage our relationships with our resident microbes. It’s more about balance and good management than defence and destruction.

They may even be able to obstruct HIV, which might explain why most infants who suckle from infected mothers don’t get infected despite drinking virus-loaded milk for months.

breast milk? German was right: it’s far more than a bag of chemicals. It nourishes baby and bacteria, infant and infantis alike. It’s a preliminary immune system that thwarts more malevolent microbes. It is the means by which a mother ensures that her children have the right companions, from their first days of life.39 And it prepares the baby for life ahead.

Around a quarter of babies in the UK and a third of those in the USA are now born by Caesarean section, many of which are elective. Maria Gloria Dominguez-Bello found that if babies are born through a cut in their mother’s abdomen, their starter microbes come from her skin and the hospital environment, instead of her vagina.24 It’s not clear what these differences mean in the long term, but just as an island’s first colonists influence the species that eventually settle upon it, the effects of a child’s first microbes could ripple through future communities. This might explain why C-section babies are more likely to develop allergies, asthma, coeliac disease, and obesity later in life. ‘The baby’s immune system is naïve at birth and whatever it sees first will start its education,’ says Dominguez-Bello. ‘Their immune system might be compromised if they start recognising the wrong guys instead of the normal good ones. It could make a difference for the rest of their life.’

Saturated fats can nourish inflammatory microbes. So can two common food additives, CMC and P80, used to lengthen the shelf life of ice cream, frozen desserts, and other processed foods; they also suppress anti-inflammatory bugs.25

But antibiotics are shock-and-awe weapons. They kill the bacteria we want as well as those we don’t – an approach that’s like nuking a city to deal with a rat. We don’t even need to see the rat to begin the massacre: many antibiotics are prescribed needlessly to treat viral infections they have no hope of countering.

One estimate suggests that the average American child gets nearly three courses of antibiotics before her second birthday, and ten before her tenth.

The blood-sucking tsetse fly, which spreads sleeping sickness between humans, also provisions its young with microbes, but does so inside its own body. It’s an insect that’s trying very hard to be a mammal. Rather than laying eggs, it gives birth to live young. And rather than hedging its bets with a horde of offspring, it devotes its energies to a single grub, which it raises inside a uterus and feeds with a milk-like fluid.

Others go for a more direct approach. 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. Many familiar animals, including cows, elephants, pandas, gorillas, rats, rabbits, dogs, iguanas, burying beetles, cockroaches, and flies, regularly eat each other’s faeces – a practice known as coprophagy.

This process, known as endosymbiosis, was first proposed in the early twentieth century, but it only became accepted several decades later, largely thanks to the outspoken American biologist Lynn Margulis. She turned endosymbiosis into a coherent theory, which she expounded in a genre-hopping paper that contained an impressive mix of evidence from cell biology, microbiology, genetics, geology, paelaeontology, and ecology. It was a bravura piece of scholarship. It was also rejected around 15 times before seeing print in 1967.21

few years ago, the Rosenbergs stumbled across an old paper from 1989, in which a biologist named 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.

The experiment was quirky but profound. If two groups of the same insect ignore each other and only mate within their social circles, they should eventually split into distinct species. These splits occur all the time in nature, and the forces that cause them can take many forms. They could be physical obstacles like mountains or rivers. They could be differences in timing, in the hours or seasons in which animals are active. They could be incompatible genes that prevent two animals from interbreeding. Anything that stops animals from mating, or that kills or weakens the offspring of those couplings, can create ‘reproductive isolation’ – a gulf that drives two species apart. And as Rosenberg had shown, bacteria can cause reproductive isolation, too. By acting as a living barrier that stops two populations from meeting up, microbes could potentially drive the origin of new species.

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.17 In other words, microbes shaped the evolution of the mammalian gut, and the shape of the mammalian gut influenced the evolution of microbes.

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 enzymes that digest the tough cellulose in the wood that termites eat.

Protists are mostly found in the guts of the earliest termite groups: the disparagingly named ‘lower termites’. The high-falutin’ ‘higher termites’ evolved later; they rely more on bacteria, which they house in a series of stomachs that are almost cow-like in their organisation.22 The even more grandiosely named macrotermites are the newest arrivals on the scene, and they have the most sophisticated strategy for destroying wood: agriculture. 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.

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...

I once went to Kenya in the middle of the great wildebeest migration – the annual marathon where millions of these cow-like antelopes travel long distances in search of greener pastures. At one point, we stopped our jeep for over half an hour to let an impossibly long line of them cross in front of us. Without microbes to extract as much nourishment as possible from tough indigestible mouthfuls, these herbivores wouldn’t exist. We wouldn’t, either. It’s hard to imagine that without domesticated ruminants, humanity would ever have gone far beyond hunting, gathering, and basic farming, much less invent international flight and safari tours. Instead of slack-jawed tourists watching a herd of fermentation chambers running past on thundering hooves, there would have been a clear horizon, and silence.

There’s a popular saying among doctors: there’s no such thing as alternative medicine; if it works, it’s just called medicine.

Petrof agrees. ‘I think everyone recognises that stool is a stopgap,’ she says. ‘We should ultimately go to defined mixtures.’ By that, she means creating a specific community of microbes that duplicates the benefits of a donor’s stool. FMT but without the F. A stool substitute. A sham-poo.

Gilbert’s team found that room-mates share more microbes than people who live apart, and couples are even more microbially similar. (‘All that I am I give to you and all that I have I share with you’, as the marriage vows go.)