5.
BEFORE ROOTS
You’ll never be free of me
He’ll make a tree from me
Don’t say good bye to me
Describe the sky to me
—TOM WAITS/KATHLEEN BRENNAN
SOMETIME AROUND SIX hundred million years ago, green algae began to move out of shallow fresh waters and onto the land. These were the ancestors of all land plants. The evolution of plants transformed the planet and its atmosphere and was one of the pivotal transitions in the history of life—a profound breakthrough in biological possibility. Today, plants make up eighty percent of the mass of all life on Earth and are the base of the food chains that support nearly all terrestrial organisms.
Before plants, land was scorched and desolate. Conditions were extreme. Temperatures fluctuated wildly and landscapes were rocky and dusty. There was nothing that we would recognize as soil. Nutrients were locked up in solid rocks and minerals, and the climate was dry. This isn’t to say that land was completely devoid of life. Crusts made up of photosynthetic bacteria, extremophile algae, and fungi were able to make a living in the open air. But the harsh conditions meant that life on Earth was overwhelmingly an aquatic event. Warm, shallow seas and lagoons teemed with algae and animals. Sea scorpions several meters long ranged the ocean floor. Trilobites plowed silty seabeds using spade-like snouts. Solitary corals started to form reefs. Mollusks thrived.
Despite its comparatively inhospitable conditions, land provided considerable opportunities for any photosynthetic organisms that could cope. Light was unfiltered by water, and carbon dioxide was more accessible—no small incentives for organisms that make a living by eating light and carbon dioxide. But the algal ancestors of land plants had no roots, no way to store or transport water, and no experience in extracting nutrients from solid ground. How did they manage the fraught passage onto dry land?
When it comes to piecing together origin stories it’s difficult to find agreement among scholars. Evidence is usually sparse, and what fragments there are can often be mobilized to support different points of view. And yet, amid the slow-burning disputes that surround the early history of life, one piece of academic consensus stands out: It was only by striking up new relationships with fungi that algae were able to make it onto land.
These early alliances evolved into what we now call “mycorrhizal relationships.” Today, more than ninety percent of all plant species depend on mycorrhizal fungi. They are the rule, not the exception: a more fundamental part of planthood than fruit, flowers, leaves, wood, or even roots. Out of this intimate partnership—complete with cooperation, conflict, and competition—plants and mycorrhizal fungi enact a collective flourishing that underpins our past, present, and future. We are unthinkable without them, yet seldom do we think about them. The cost of our neglect has never been more apparent. It is an attitude we can’t afford to sustain.
AS WE’VE SEEN, algae and fungi have a tendency to partner with one another. Their association can take many forms. Lichens are one example. Seaweeds—also algae—are another; many seaweeds washed up on shorelines depend on fungi to nourish them and prevent them from drying out. And then there are the soft green balls produced in days by the Harvard researchers when they introduced free-living fungi and algae to one another. As long as fungi and algae have a good ecological fit—as long as they sing a metabolic “song” together that neither can sing alone—they will coalesce into entirely new symbiotic relationships. In this sense, the union of fungi and algae that gave rise to plants is part of a larger story, an evolutionary refrain.
Whereas the partners in lichens come together to make a body altogether unlike those of their individual members, the partners in a mycorrhizal relationship do not: Plants stay recognizable as plants, and mycorrhizal fungi stay recognizable as fungi. This makes for a very different, more promiscuous type of symbiosis in which a single plant can be coupled to many fungi at once, and a single fungus can be coupled to many plants.
For the relationship to thrive, both plant and fungus must make a good metabolic match. It is a familiar pact. In photosynthesis, plants harvest carbon from the atmosphere and forge the energy-rich carbon compounds—sugars and lipids—on which much of the rest of life depends. By growing within plant roots, mycorrhizal fungi acquire privileged access to these sources of energy: They get fed. However, photosynthesis isn’t enough to support life. Plants and fungi need more than a source of energy. Water and minerals must be scavenged from the ground—full of textures and micropores, electrically charged cavities, and labyrinthine rotscapes. Fungi are deft rangers in this wilderness and can forage in a way that plants can’t. By hosting fungi within their roots, plants gain hugely improved access to these sources of nutrients. They, too, get fed. By partnering, plants gain a prosthetic fungus, and fungi gain a prosthetic plant. Both use the other to extend their reach. It is an example of Lynn Margulis’s “long-lasting intimacy of strangers.” Except that they’re hardly strangers anymore. Look inside a root, and this becomes clear.
Roots turn into worlds under a microscope. I’ve spent weeks immersed in them, sometimes enthralled, sometimes frustrated. Put fresh, fine roots in a dish of water and you’ll see fungal hyphae stringing off them. Boil roots in dye, squash them onto a glass slide, and you’ll see an intertwining. Fungal hyphae fork and fuse and erupt within plant cells in a riot of branching filaments. Plant and fungus clasp one another. It’s difficult to imagine a more intimate set of poses.
The strangest thing I’ve seen under a microscope is germinating dust seeds. Dust seeds are the smallest plant seeds in the world. A single seed is just visible to the naked eye like a small hair or the tip of an eyelash. Orchids make them, as do some other plants. They weigh almost nothing and disperse easily with wind or rain. And they won’t germinate until they’ve met a fungus. I spent a long time trying to catch them in the act. I buried thousands of dust seeds in small bags and dug them up after a few months hoping that some would have sprouted. Under the microscope I pushed seeds around a glass dish with a needle searching for signs of life. After several days, I found what I was looking for. Some seeds had swollen into fleshy clumps tangled up in fungal hyphae, sticky streamers that trailed out into the dish. Inside the developing roots, hyphae raveled into knots and coils. This wasn’t sex: Fungal and plant cells hadn’t fused and pooled their genetic information. But it was sexy: Cells from two different creatures had met, incorporated each other, and were collaborating in the building of a new life. To imagine the future plant as separable from the fungus was absurd.
IT ISN’T CLEAR how mycorrhizal relationships first arose. Some venture that the earliest encounters were soggy, disorganized affairs: fungi seeking food and refuge within algae that washed up onto the muddy shores of lakes and rivers. Some propose instead that the algae arrived on land with their fungal partners already in tow. Either way, explained Katie Field, a professor at the University of Leeds, “they soon became dependent on each other.”
Field is a brilliant experimentalist who has spent years studying the most ancient lineages of plants alive today. Using radioactive tracers, she measures the exchanges taking place between fungi and plants in growth chambers that simulate ancient climates. Their symbiotic manners provide clues about how plants and fungi behaved toward one another in the earliest stages of their migration onto land. Fossils, too, provide a striking glimpse of these early alliances. The finest specimens date from around four hundred million years ago and bear the unmistakable imprint of mycorrhizal fungi within them: feathery lobes that look just as they do today. “You can see the fungus actually living in the plant cells,” Field marveled.
The earliest plants were little more than puddles of green tissue, with no roots or other specialized structures. Over time, they evolved coarse fleshy organs to house their fungal associates, who scavenged the soil for nutrients and water. By the time the first roots evolved, the mycorrhizal association was already some fifty million years old. Mycorrhizal fungi are the roots of all subsequent life on land. The word mycorrhiza has it right. Roots (rhiza) followed fungi (mykes) into being.
Today, hundreds of millions of years later, plants have evolved thinner, faster-growing, opportunistic roots that behave more like fungi. But even these roots can’t outmaneuver fungi when it comes to exploring the soil. Mycorrhizal hyphae are fifty times finer than the finest roots and can exceed the length of a plant’s roots by as much as a hundred times. They came before roots, and range beyond roots. Some researchers take it further. “Plants don’t have roots,” one of my undergraduate professors confided to a class of astounded students. “They have fungus-roots, myco-rhizas.”
Mycorrhizal fungi are so prolific that their mycelium makes up between a third and a half of the living mass of soils. The numbers are astronomical. Globally, the total length of mycorrhizal hyphae in the top ten centimeters of soil is around half the width of our galaxy (4.5 × 1017 kilometers of hyphae, versus 9.5 × 1017 kilometers of space). If these hyphae were ironed into a flat sheet, their combined surface area would cover every inch of dry land on Earth two and a half times over. However, fungi don’t stay still. Mycorrhizal hyphae die back and regrow so rapidly—between ten and sixty times per year—that over a million years their cumulative length would exceed the diameter of the known universe (4.8 × 1010 light years of hyphae, versus 9.1 × 109 light years in the known universe). Given that mycorrhizal fungi have been around for some five hundred million years and aren’t restricted to the top ten centimeters of soil, these figures are certainly underestimates.
In their relationship, plants and mycorrhizal fungi enact a polarity: Plant shoots engage with the light and air, while the fungi and plant roots engage with the solid ground. Plants pack up light and carbon dioxide into sugars and lipids. Mycorrhizal fungi unpack nutrients bound up in rock and decomposing material. These are fungi with a dual niche: Part of their life happens within the plant, part in the soil. They are stationed at the entry point of carbon into terrestrial life cycles and stitch the atmosphere into relation with the ground. To this day, mycorrhizal fungi help plants cope with drought, heat, and the many other stresses life on land has presented from the very beginning, as do the symbiotic fungi that crowd into plant leaves and stems. What we call “plants” are in fact fungi that have evolved to farm algae, and algae that have evolved to farm fungi.
Mycorrhizal fungus inside a plant root
THE WORD mycorrhiza was coined in 1885 by the German biologist Albert Frank—the same Albert Frank whose fascination with lichens had led him to coin the word symbiosis eight years earlier. He was subsequently employed by the Ministry of Agriculture, Domains and Forestry for the Kingdom of Prussia, to “promote the possibility of truffle cultivation,” a post that caused him to turn his attention toward the soil. As for many before and since, truffles were the lure that tugged him into a fungal underground.
Frank didn’t have much success in cultivating truffles, but in his inquiries, he documented in vivid detail the entanglement between tree roots and the mycelium of truffle fungi. His diagrams portray root tips entangled within a mycelial sleeve, with hyphae writhing outward onto the page. Frank was struck by the intimacy of the association, and suggested that the relationship between plant roots and their companion fungi might be mutually beneficial rather than parasitic. As was common among scientists studying symbiosis, Frank used lichens as an analogy to make sense of the mycorrhizal association. In his view, plants and mycorrhizal fungi were bound in an “intimate, reciprocal dependence.” Mycorrhizal mycelium behaved like a “wet nurse,” and enabled “the entire nourishment of the tree from the soil.”
Frank’s ideas were fiercely attacked, as Simon Schwendener’s dual hypothesis of lichens had been. For Frank’s critics, the idea that the symbiosis could be of mutual benefit—a “mutualism”—was a sentimental illusion. If one partner appeared to benefit, they did so at a price. Any symbiosis that appeared to be mutually beneficial was actually one of conflict and parasitism in disguise. Undeterred, Frank worked for ten years to understand plants’ relationships with their fungal “nurses.” He performed elegant experiments with pine seedlings. Some he grew in sterilized soil; some he grew in soil collected from a nearby pine forest. Those that grew in forest soil formed fungal relationships and developed into larger, healthier saplings than those grown in sterile conditions.
Frank’s findings caught the eye of J.R.R. Tolkien, who had a well-known fondness for plants, and trees in particular. Mycorrhizal fungi soon found their way into The Lord of the Rings.
“For you little gardener and lover of trees,” said the elf Galadriel to the hobbit Sam Gamgee, “I have only a small gift…In this box there is earth from my orchard…if you keep it and see your home again at last, then perhaps it may reward you. Though you should find all barren and laid waste, there will be few gardens in Middle-earth that will bloom like your garden, if you sprinkle this earth there.”
When he finally returned home to find a devastated Shire:
Sam Gamgee planted saplings in all the places where specially beautiful or beloved trees had been destroyed, and he put a grain of the precious dust from Galadriel in the soil at the root of each…All through the winter he remained as patient as he could, and tried to restrain himself from going round constantly to see if anything was happening. Spring surpassed his wildest hopes. His trees began to sprout and grow, as if time was in a hurry and wished to make one year do for twenty.
TOLKIEN COULD HAVE been describing plant growth in the Devonian period, three hundred to four hundred million years ago. By now well-established on land, and fueled by high levels of light and carbon dioxide, plants spread across the world and evolved larger and more complex forms faster than at any time before. Meter-tall trees evolved into thirty-meter-tall trees in a few million years. Over this period, as plants boomed, the amount of carbon dioxide in the atmosphere dropped by ninety percent, triggering a period of global cooling. Could plants and their fungal associates have played a part in this massive atmospheric transformation? A number of researchers, Field included, think it’s probable.
“The levels of carbon dioxide in the atmosphere drop off dramatically at the same time as land plants are evolving increasingly complex structures,” Field explained. The surge in plant productivity in turn depended on their mycorrhizal partners. It’s a predictable sequence of events. One of the biggest limits to plant growth is a scarcity of the nutrient phosphorus. One of the things that mycorrhizal fungi do best—one of their most prominent metabolic “songs”—is to mine phosphorus from the soil and transfer it to their plant partners. If plants are fertilized with phosphorus, they grow more. The more plants grow, the more they draw down carbon dioxide from the atmosphere. The more plants live, the more plants die, and the more carbon is buried in soils and sediments. The more carbon that is buried, the less there is in the atmosphere.
Phosphorus is only part of the story. Mycorrhizal fungi deploy acids and high pressure to burrow into solid rock. With their help, plants in the Devonian period were able to mine minerals like calcium and silica. Once unlocked, these minerals react with carbon dioxide, pulling it out of the atmosphere. The resulting compounds—carbonates and silicates—find their way into the oceans where they are used by marine organisms to make their shells. When the organisms die, the shells sink and pile up hundreds of meters thick on the ocean floor, which becomes an enormous burial ground for carbon. Add all of this up and climates start to change.
Is there a way to measure the impact of mycorrhizal fungi on ancient global climates, I wondered. “Yes and no,” Field replied. “I recently tried.” To do so, she collaborated with the biogeochemist Benjamin Mills, a fellow researcher at the University of Leeds, who works with computer models that give predictions about the climate and the composition of the atmosphere.
Lots of researchers build climate models. Weather forecasters and climate scientists depend on these digital simulations to predict future scenarios. So do researchers trying to reconstruct major transitions in the planet’s past. By varying the numbers dialed into the model, one can test different hypotheses about the history of the Earth’s climate. Turn up carbon dioxide, and what happens? Turn down the amount of phosphorus that plants can access and what happens? The model can’t say what actually occurred, but it can tell us which factors are capable of making a difference.
Before Field approached him, Mills hadn’t included mycorrhizal fungi in the model. He could vary the amount of phosphorus that plants could obtain. However, without taking account of mycorrhizal fungi, there is no way to make realistic estimates of how much phosphorus plants were able to access. Field could help. In a series of experiments, she had found that the outcome of mycorrhizal relationships varied depending on the climatic conditions in her growth chambers. Sometimes plants benefited more from the relationship, and sometimes less, a trait she terms “symbiotic efficiency.” If plants are hitched to an efficient mycorrhizal partner, they receive more phosphorus and grow more. Field was able to estimate how efficient mycorrhizal exchange would have been around 450 million years ago, when atmospheric carbon dioxide levels were several times higher than they are today.
When Mills added mycorrhizal fungi to the model using Field’s measurements, he found that it was possible to change the entire global climate simply by turning the symbiotic efficiency up or down. The amount of carbon dioxide and oxygen in the atmosphere, and global temperatures—all varied according to the efficiency of mycorrhizal exchange. Based on Field’s data, mycorrhizal fungi would have made a substantial contribution to the dramatic drawdown of carbon dioxide that followed the plant boom in the Devonian period. “It’s one of those moments where you think: Wow, actually, hang on!” Field exclaimed. “Our results suggest that mycorrhizal relationships have played a role in the evolution of much of life on Earth.”
THEY CONTINUE TO do so. The book of Isaiah in the Old Testament has it that “all flesh is grass.” It is a logic that we might today describe as ecological: In animal bodies, grass becomes flesh. But why stop there? Grass only becomes grass when sustained by the fungi that live in its roots. Does this mean that all grass is fungus? If all grass is fungus, and all flesh is grass, does it follow that all flesh is fungus?
Maybe not all, but certainly some: Mycorrhizal fungi can provide up to eighty percent of a plant’s nitrogen and as much as a hundred percent of its phosphorus. Fungi supply other crucial nutrients to plants, such as zinc and copper. They also provide plants with water, and help them to survive drought as they’ve done since the earliest days of life on land. In return, plants allocate up to thirty percent of the carbon they harvest to their mycorrhizal partners. Exactly what is taking place between a plant and mycorrhizal fungus at any given moment depends on who’s involved. There are many ways to be a plant, and many ways to be a fungus. And there are many ways to form a mycorrhizal relationship: It is a way of life that has evolved on more than sixty separate occasions in different fungal lineages since algae first migrated onto land. As with many traits that have defied the odds to evolve more than once—whether the ability to hunt nematodes, form lichens, or manipulate animal behavior—it is hard to avoid the feeling that these fungi have stumbled upon a winning strategy.
A plant’s fungal partners can have a noticeable impact on its growth—and its flesh. A number of years ago, at a conference on mycorrhizal relationships, I met a researcher who had been growing strawberry plants with different communities of mycorrhizal fungus. The experiment was simple. If the same species of strawberry was grown with different species of fungus, would the flavor of the strawberries change? He conducted blind taste tests and found that different fungal communities did seem to change the flavor of the fruit. Some had more flavor, some were juicier, some were sweeter.
When he repeated the experiment a second year running, unpredictable weather swamped the effects of mycorrhizal fungi on the taste of the strawberries, but a number of other striking effects surfaced. Bumblebees were more attracted to the flowers of strawberry plants grown with some fungal species and less attracted to others. Plants grown with some mycorrhizal species produced more berries than others. And the appearance of the berries changed depending on which fungi they partnered with. Some mycorrhizal communities made the berries look more appealing, some less so.
Strawberries aren’t alone in being sensitive to the identity of their fungal partners. Most plants—from a potted snapdragon to a giant sequoia—will develop differently when grown with different communities of mycorrhizal fungus. Basil plants, for example, produce different profiles of the aromatic oils that make up their flavor when grown with different mycorrhizal strains. Some fungi have been found to make tomatoes sweeter than others; some change the essential oil profile of fennel, coriander, and mint; some increase the concentration of iron and carotenoids in lettuce leaves, the antioxidant activity in artichoke heads, or the concentrations of medicinal compounds in Saint-John’s-wort and echinacea. In 2013, a team of Italian researchers baked loaves of bread using wheat that had been grown with different mycorrhizal communities. The bread was subjected to testing with an electronic nose and a tasting panel consisting of ten “well-trained testers” at the University of Gastronomic Sciences in Bra, Italy. (Each tester, the authors assert reassuringly, “had a minimum of two years’ experience in sensory evaluation.”) Surprisingly, given how many stages occur between harvest and tasting—milling, mixing, and baking, besides the addition of yeast—both the panel and the electronic nose were able to tell the loaves apart. The bread grown with an enhanced mycorrhizal fungal community had a higher “flavor intensity” and improved “elasticity and crumbliness.” By smelling a flower, by chewing on twigs, leaves, or bark, by drinking a wine, how many other aspects of a plant’s mycorrhizal underground might we be able to taste? I often wonder.
Mycorrhizal root tip
“HOW DELICATE IS the mechanism by which the balance of power is maintained among members of the soil population,” reflected the mycologist Mabel Rayner in Trees and Toadstools, a book on mycorrhizal relationships, published in 1945. Different species of mycorrhizal fungus might cause a basil leaf to taste different or a strawberry plant to produce more delicious-looking berries. But how? Are some fungal partners “better” than others? Are some plant partners “better” than others? Can plants and fungi tell the difference between alternative partners? Decades have elapsed since Rayner’s remark, but we are only just beginning to understand the intricate behaviors that maintain a symbiotic balance between plants and mycorrhizal fungi.
Social interactions are demanding. According to some evolutionary psychologists, humans’ large brains and flexible intellects arose to allow us to navigate our way through complex social situations. Even the smallest interaction is embedded within a shifting social constellation. According to the Chambers Dictionary of Etymology, the word entangle was originally used to describe such human interactions, or our involvement in “complex affairs.” Not until later did the word take on other meanings. We humans became as clever as we are, so the argument goes, because we were entangled within a demanding flurry of interaction.
Plants and mycorrhizal fungi don’t have recognizable brains or intellects, but they certainly live entangled lives and have had to evolve ways to manage their complex affairs. Plants’ actions are informed by what is happening in the sensory world of their fungal partners. Similarly, fungal behaviors are informed by what is happening in the sensory world of their plant partners. Using information from between fifteen and twenty different senses, a plant’s shoots and leaves explore the air and adjust their behavior based on continuous subtle changes in their surroundings. Anywhere from thousands to billions of root tips explore the soil, each able to form multiple connections to different fungal species. Meanwhile, a mycorrhizal fungus must sniff out sources of nutrients, proliferate within them, mingle with crowds of other microbes—whether fungal, bacterial, or other—absorb the nutrients, and divert them around its rambling network of a body. Information must be integrated across an immense number of hyphal tips, which at any one moment can be strung between several different plants and sprawl over tens of meters.
Toby Kiers, a professor at Vrije Universiteit Amsterdam, is one of the researchers who has done the most to investigate how plants and fungi maintain their “balance of power.” Using radioactive labels, or by attaching light-emitting tags to molecules, she and her team are able to trace the carbon that moves from plant roots into fungal hyphae, and phosphorus that moves from fungi into plant roots. By carefully measuring these fluxes, she has been able to describe some of the ways in which both partners manage their exchange. How do plants and mycorrhizal fungi navigate their demanding social landscapes, I asked Kiers. She laughed. “We really want to get our hands on the complexity of what’s happening. We know that trade is taking place. The question is whether we can predict how trading strategies change. It’s overwhelming, but why not try?”
Kiers’s findings are surprising because they suggest that neither plant nor fungus is in complete control of the relationship. Between them, they are able to strike compromises, resolve trade-offs, and deploy sophisticated trading strategies. In one set of experiments, she found that plant roots were able to supply carbon preferentially to fungal strains that provided them with more phosphorus. In return, fungi that received more carbon from the plant supplied it with yet more phosphorus. Exchange was in some sense negotiated between the two depending on the availability of resources. Kiers hypothesized that these “reciprocal rewards” have helped to keep plant and fungal associations stable over evolutionary time. Because both partners share control of the exchange, neither partner would be able to hijack the relationship for their own exclusive benefit.
Although both plants and fungi tend to benefit from the relationship overall, different species of plant and fungus have different symbiotic manners. Some fungi make more cooperative partners; some are less cooperative and will “hoard” phosphorus rather than exchange it with their plant partners. However, even a hoarder might not hoard all the time. Their behavior is flexible, a set of ongoing negotiations that depend on what is taking place around them and in other parts of themselves. We don’t know much about the workings of these behaviors, but it’s clear that at any one moment plants and fungi face a number of options. And options entail choices, however those choices turn out to be made—whether in a conscious human mind, an unconscious computer algorithm, or anything in between.
Are plants and fungi making decisions, albeit brainless ones, I wondered. “I use the word decision all the time,” Kiers told me. “There’s a set of options, and somehow information has to be integrated and one of the options has to be chosen. I think that a lot of what we are doing is studying micro-scale decisions.” There are many ways that these choices could unfold. “Are there absolute decisions being made in every hyphal tip?” Kiers mused. “Or is it all relative, in which case what happens would depend on what else is happening across the network.”
Intrigued by these questions, and having read Thomas Piketty’s work on wealth inequality in human societies, Kiers began thinking about the role of inequality within fungal networks. She and her team exposed a single mycorrhizal fungus to an unequal supply of phosphorus. One part of the mycelium had access to a big patch of phosphorus. Another part had access to a small patch. She was interested in how this would affect the fungus’s trading decisions in different parts of the same network. Some recognizable patterns emerged. In parts of a mycelial network where phosphorus was scarce, the plant paid a higher “price,” supplying more carbon to the fungus for every unit of phosphorus it received. Where phosphorus was more readily available, the fungus received a less favorable “exchange rate.” The “price” of phosphorus seemed to be governed by the familiar dynamics of supply and demand.
Most surprising was the way that the fungus coordinated its trading behavior across the network. Kiers identified a strategy of “buy low, sell high.” The fungus actively transported phosphorus—using its dynamic microtubule “motors”—from areas of abundance, where it fetched a low price when exchanged with a plant root, to areas of scarcity, where it was in higher demand and fetched a higher price. By doing so, the fungus was able to transfer a greater proportion of its phosphorus to the plant at the more favorable exchange rate, thus receiving larger quantities of carbon in return.
How are these behaviors controlled? Can the fungus detect differences in exchange rate across its network and actively transport phosphorus to play the system? Or does it always transport phosphorus within its network from areas of abundance to areas of scarcity, sometimes receiving a payoff from the plant, and sometimes not? We still don’t know. Nonetheless, Kiers’s studies illuminate some of the intricacies of plant and fungal exchange, and show how solutions to complex challenges are able to emerge. All of these behaviors illustrate a general pattern. How a given plant or fungus behaves depends on who they find themselves partnering with and where they happen to be. One can think of mycorrhizal relationships as stretched along a continuum, with parasites at one pole and cooperative mutualists at the other. Some plants benefit from their fungal partners under some conditions and not under others. Grow plants with plenty of phosphorus, and they might become less picky about which fungal species they partner with. Grow cooperative fungi alongside other cooperative fungi, and they might become less cooperative. Same fungus, same plant, different setting, different outcome.
ONE OF MY collaborators, a professor at the University of Marburg, told me about a sculpture he had seen as a child. The Vertical Earth Kilometer is a brass pole one kilometer long buried in the ground. The only visible part of it is the very end of the pole: a brass circle that lies flat on the floor and looks like a coin. He described the imaginative vertigo it had triggered in him, the sense of floating on the surface of an ocean of land, looking down into its depths. The experience inspired his lifelong fascination with roots and mycorrhizal fungi. I feel a similar sense of vertigo when I think about the complexity of mycorrhizal relationships—kilometers of entangled life—jostling beneath my feet.
The vertigo really sets in when I try to scale from the very small to the very large, from the microscopic trading decisions taking place at a cellular level, up to the entire planet, the atmosphere, the three-trillion-odd trees that make their lives on land, and the quadrillions of miles of mycorrhizal fungi that weave them into relation with the soil. Our minds aren’t good at keeping their balance when faced with numbers this big. Yet the story of mycorrhizal relationships makes many such dizzying swoops, from very large to very small and back again.
Scale is an issue in the field of mycorrhizal research. Mycorrhizal relationships are conducted out of sight. It is hard to experience them, to see them or touch them. Their inaccessibility means that most knowledge of mycorrhizal behavior comes from studies in controlled laboratory or greenhouse settings. Scaling up these findings to complex real-world ecosystems isn’t always possible. Much of the time we only see a small part of the picture. The result is that researchers know more about what mycorrhizal fungi are capable of doing than what they’re actually doing.
Even in controlled settings, it’s difficult to get a feel for how mycorrhizal fungi actually behave on a moment-to-moment basis. By contrast with Kiers’s studies, there are situations in which plant and fungal exchanges don’t seem to obey what we would recognize as rational trading strategies. Is something missing from our understanding? No one can be sure. We have very little idea of exactly how the chemical exchange between plants and fungi takes place, and how it is controlled at a cellular level. “We’re trying to study how stuff moves within a network,” Kiers told me. “We’re trying to get videos of it. It’s so crazy what’s going on in there. But these studies are hard, and I can understand why people would want to work with different organisms.” Many mycologists share this combination of excitement and frustration.
Are there other ways to think about these associations, other ways to quell the vertigo? Some of my colleagues find more intuitive outlets for their mycorrhizal enthusiasm. A number of them are passionate mushroom hunters. By foraging for mushrooms—from truffle to porcini to chanterelle to matsutake—they involve themselves with mycorrhizal relationships in a more spontaneous way. Others spend hours looking at mycorrhizal fungi under microscopes, which is almost the equivalent of a marine biologist going for a dive. Some of them spend hours sifting mycorrhizal spores from the soil, colorful orbs that under the microscope glisten like fish eggs. One of my colleagues in Panama was a skilled spore wrangler. Some evenings we made snacks from spores, fragments of cracker, and sour cream: tiny crumbs of mycorrhizal caviar that we had to prepare under the microscope and tweezer into our mouths. We didn’t learn much, but that wasn’t the point. It was an exercise that helped us to keep our balance as we careened from the small to the large. These were rare moments of unmediated contact with our experimental subjects, goofs to remind us that mycorrhizal fungi aren’t mechanical schematic entities—one can’t eat a machine or a concept—but living organisms engaged in lives that we still struggle to understand.
PLANTS REMAIN THE easiest way in. It is through plants that the mycorrhizal extravaganza belowground most commonly erupts into everyday human life. The countless microscopic interactions that occur between fungi and roots express themselves in the forms, growth, tastes, and smells of plants. Sam Gamgee, like Albert Frank, could see the outcome of young trees’ mycorrhizal relationships with his own eyes: The saplings “began to sprout and grow, as if time was in a hurry.” Eat a plant, and we taste the outgrowth of a mycorrhizal relationship. Cultivate plants—in a plant pot, flower bed, garden, or city park—and we cultivate mycorrhizal relationships. Scale up yet further, and the microscopic trading decisions made by plants and fungi can shape the populations of forests across entire continents.
The last Ice Age ended around eleven thousand years ago. As the vast Laurentide Ice Sheet retreated, it revealed millions of square kilometers of North America. Over a period of several thousand years, forests expanded northward. Using pollen records, it is possible to reconstruct the migration timelines of different species of tree. Some—beech, alder, pine, fir, maple—moved quickly, more than a hundred meters per year. Some—plane, oak, birch, hickory—moved more slowly, around ten meters per year.
What was it about these different species that determined their response to the changing climate? The relationship between fungi and the ancestors of plants allowed them to migrate onto dry land. Could mycorrhizal relationships have continued to play a part in plants’ movements around the planet hundreds of millions of years later? It’s possible. Neither plants nor fungi inherit each other. They inherit a tendency to associate, but they conduct what are, by the standards of many other ancient symbioses, open relationships. As in the earliest days of life on land, plants form their relationships depending on who’s around. The same goes for fungi. Though this might be a limitation—a plant seed that finds no compatible fungi is unlikely to survive—the ability to reform their relationships, or evolve entirely new ones, can allow partners to respond to changing circumstances. A study published in 2018 by researchers at the University of British Columbia found that the speed of tree migration may indeed depend on their mycorrhizal proclivity. Some species of tree are more promiscuous than others and can enter into relationships with many different fungal species. As the Laurentide Ice Sheet retreated, the species that migrated faster were the more promiscuous ones, those that stood a better chance of meeting a compatible fungus when they arrived somewhere new.
The fungi that live in plant leaves and shoots—known as “endophytes”—can have similarly dramatic effects on a plant’s ability to make a life in a new place. Take a grass from salty coastal soils, grow it without its fungal endophytes, and it won’t be able to survive in its natural salty habitat. The same goes for grasses growing in hot geothermal soils. Researchers swapped the fungal endophytes that lived in each type of grass so that coastal grasses were grown with hot geothermal fungi and vice versa. The grasses’ ability to survive in each habitat switched. Coastal grasses could no longer grow in salty coastal soils but thrived in hot geothermal soils. Hot geothermal grasses could no longer grow in the hot geothermal soils but thrived in the salty coastal soils.
Fungi can determine which plants grow where; they can even drive the evolution of new species by isolating plant populations from one another. Lord Howe Island is nine kilometers long, around a kilometer wide, and lies between Australia and New Zealand. On it grow two species of palm that have diverged from each other. One species, the Belmore sentry palm (Howea belmoreana), grows on acidic volcanic soils, while its sister species, the Kentia palm (Howea forsteriana), lives on alkaline chalky soils. What enabled the Kentia palm’s radical switch of habitats has long puzzled botanists. A study published in 2017 by researchers at Imperial College London shows that mycorrhizal fungi are largely responsible. They found that the two palm species associate with different fungal communities. The Kentia palm is able to form relationships with fungi that allow it to live on the alkaline chalky soils. However, its ability to do so makes it difficult to form relationships with the mycorrhizal fungi in the ancestral volcanic soils. This means that the Kentia palm benefits only from the fungi present in the chalky soils, whereas the Belmore sentry palm benefits only from the fungi present in the volcanic soils. Over time, living on different mycorrhizal “islands,” though sharing the same tiny geographical island, one species became two.
The ability of plants and mycorrhizal fungi to reshape their relationships has profound implications. We are familiar with the story: Throughout human history, partnerships with other organisms have extended the reach of both humans and nonhumans. Human relationships with corn brought about new forms of civilization. Relationships with horses allowed new forms of transport. Relationships with yeast permitted new forms of alcohol production and distribution. In each case, humans and their nonhuman partners redefined their possibilities.
Horses and humans remain separate organisms, as do plants and mycorrhizal fungi, but both are echoes of an ancient tendency for organisms to associate. The anthropologists Natasha Myers and Carla Hustak argue that the word evolution, which literally means “rolling outward,” doesn’t capture the readiness of organisms to involve themselves in one another’s lives. Myers and Hustak suggest that the word involution—from the word involve—better describes this tendency: a “rolling, curling, turning inward.” In their view, the concept of involution better captures the entangled pushing and pulling of “organisms constantly inventing new ways to live with and alongside one another.” It was their tendency to involve themselves in the lives of others that enabled plants to borrow a root system for fifty million years while they evolved their own. Today, even with their own root systems, almost all plants still depend on mycorrhizal fungi to manage their underground lives. Their involutionary tendencies enabled fungi to borrow a photosynthesizing alga to handle their atmospheric affairs. They still do. Mycorrhizal fungi are not built into plant seeds. Plants and fungi must constantly form and re-form their relationships. Involution is ongoing and extravagant: By associating with one another, all participants wander outside and beyond their prior limits.
Faced with catastrophic environmental change, much of life depends on the ability of plants and fungi to adapt to new conditions, whether in polluted or deforested landscapes or in newly created environments such as urban green roofs. Increases in atmospheric carbon dioxide, changes in climate, and pollution all influence the microscopic trading decisions of plant roots and their fungal partners. As has long been the case, the influences of these trading decisions scale up and spill out over whole ecosystems and landmasses. A large study published in 2018 suggested that the “alarming deterioration” of the health of trees across Europe was caused by a disruption of their mycorrhizal relationships, brought about by nitrogen pollution. Mycorrhizal associations born of the Anthropocene will determine much of humans’ ability to adapt to the worsening climate emergency. Nowhere are the possibilities—and pitfalls—more apparent than in agriculture.
“ON THE EFFICIENCY of this mycorrhizal association the health and well-being of mankind must depend.” So wrote Albert Howard, a founding figure in the modern organic farming movement and a passionate spokesman for mycorrhizal fungi. In the 1940s, Howard argued that the widespread application of chemical fertilizers would disrupt mycorrhizal associations, the means by which “the marriage of a fertile soil and the tree it nourishes…is arranged.” The consequences of such a breakdown would be far-reaching. To cut these “living fungous threads” would be to reduce the health of the soil. In turn, the health and productivity of crops would suffer, as would the animals and people that consumed them. “Can mankind regulate its affairs so that its chief possession—the fertility of the soil—is preserved?” Howard challenged. “On the answer to this question the future of civilization depends.”
Howard’s tone is dramatic, but eighty years on his questions cut deep. By some measures, modern industrial agriculture has been effective: Crop production doubled over the second half of the twentieth century. But a single-minded focus on yield has incurred steep costs. Agriculture causes widespread environmental destruction and is responsible for a quarter of global greenhouse gas emissions. Between twenty and forty percent of crops are lost each year to pests and diseases, despite colossal applications of pesticides. Global agricultural yields have plateaued, despite a seven-hundred-fold increase in fertilizer use over the second half of the twentieth century. Worldwide, thirty football fields’ worth of topsoil are lost to erosion every minute. Yet a third of food is wasted, and demand for crops will double by 2050. It is difficult to overstate the urgency of the crisis.
Could mycorrhizal fungi form part of the solution? Perhaps it’s a silly question. Mycorrhizal relationships are as old as plants and have been shaping Earth’s future for hundreds of millions of years. They have forever featured in our efforts to feed ourselves, whether we’ve thought about them or not. For millennia in many parts of the world, traditional agricultural practices have attended to the health of the soil, and thus supported plants’ fungal relationships implicitly. But over the course of the twentieth century, our neglect has led us into trouble. In 1940, Howard’s greatest worry was that industrial agricultural techniques would develop without taking account of the “life of the soil.” His concern was justified. In viewing soils as more or less lifeless places, agricultural practices have ravaged the underground communities that sustain the life we eat. There are parallels with much of twentieth-century medical science, which considered “germ” and “microbe” to mean the same thing. Of course some soil organisms, like some microbes that live on your body, can cause disease. Most do quite the opposite. Disrupt the ecology of microbes that live in your gut, and your health will suffer—a growing number of human diseases are known to arise because of efforts to rid ourselves of “germs.” Disrupt the rich ecology of microbes that live in the soil—the guts of the planet—and the health of plants, too, will suffer.
A study published in 2019 by researchers at Agroscope in Zurich measured the scale of the disruption by comparing the impact of organic and conventional “intensive” farming practices on fungal communities in the roots of crops. By sequencing fungal DNA, the authors were able to compile networks showing which fungal species associated with one another. They found “remarkable differences” between organic and conventionally managed fields. Not only was the abundance of mycorrhizal fungi higher in organically managed fields but the fungal communities were also far more complex: Twenty-seven species of fungi were identified as highly connected, or “keystone species,” compared with none in the conventionally managed fields. Many studies report similar findings. Intensive farming practices—through a combination of plowing and application of chemical fertilizers or fungicides—reduce the abundance of mycorrhizal fungi and alter the structure of their communities. More sustainable farming practices, organic or otherwise, tend to result in more diverse mycorrhizal communities and a greater abundance of fungal mycelium in the soil.
Does it matter? Much of the story of agriculture is one of ecological sacrifice. Forests are cleared to make way for fields. Hedgerows are cleared to make way for bigger fields. Surely it is the same with the communities of microbes in the soil? If humans feed crops by adding fertilizer to fields, don’t we take over the job of mycorrhizal fungi? Why care about the fungi if we have made them redundant?
Mycorrhizal fungi do more than feed plants. The researchers at Agroscope describe them as keystone organisms but some prefer the term “ecosystem engineers.” Mycorrhizal mycelium is a sticky living seam that holds soil together; remove the fungi, and the ground washes away. Mycorrhizal fungi increase the volume of water that the soil can absorb, reducing the quantity of nutrients leached out of the soil by rainfall by as much as fifty percent. Of the carbon that is found in soils—which, remarkably, amounts to twice the amount of carbon found in plants and the atmosphere combined—a substantial proportion is bound up in tough organic compounds produced by mycorrhizal fungi. The carbon that floods into the soil through mycorrhizal channels supports intricate food webs. Besides the hundreds or thousands of meters of fungal mycelium in a teaspoon of healthy soil, there are more bacteria, protists, insects, and arthropods than the number of humans who have ever lived on Earth.
Mycorrhizal fungi can increase the quality of a harvest, as the experiments with basil, strawberries, tomatoes, and wheat illustrate. They can also increase the ability of crops to compete with weeds and enhance their resistance to diseases by priming plants’ immune systems. They can make crops less susceptible to drought and heat, and more resistant to salinity and heavy metals. They even boost the ability of plants to fight off attacks from insect pests by stimulating the production of defensive chemicals. The list goes on: The literature is awash with examples of the benefits that mycorrhizal relationships provide to plants. However, putting this knowledge into practice is not always straightforward. For one thing, mycorrhizal associations don’t always increase crop yields. In some cases, they can even reduce them.
Katie Field is one of the many researchers being funded to develop mycorrhizal solutions to agricultural problems. “The whole relationship is much more plastic and affected by the environment than we thought,” she told me. “A lot of the time the fungi aren’t helping the crops take up nutrients. The results are super variable. It totally depends on the type of fungus, the type of plant, and the environment in which it’s growing.” A number of studies report similarly unpredictable outcomes. Most modern crop varieties have been developed with little thought for their ability to form high-functioning mycorrhizal relationships. We’ve bred strains of wheat to grow fast when they are given lots of fertilizer, and ended up with “spoiled” plants that have almost lost the ability to cooperate with fungi. “The fact that the fungi are colonizing these cereal crops at all is a minor miracle,” Field pointed out.
The subtleties of mycorrhizal relationships mean that the most obvious intervention—supplementing plants with mycorrhizal fungi and other microbes—can cut two ways. Sometimes, as Sam Gamgee found, introducing plants to a community of soil microbes can support the growth of crops and trees and help restore life to devastated soils. However, the success of this approach depends on the ecological fit. Poorly matched mycorrhizal species might do more harm to plants than good. Worse, introducing opportunistic fungal species to new environments might displace local fungal strains with unknown ecological consequences. It is a fact not always taken into account by the fast-growing industry of commercial mycorrhizal products, often marketed as one-size-fits-all quick fixes. As in the ballooning market for human probiotics, many of the microbial strains sold are selected not because they are particularly suitable but because they are easy to produce in manufacturing facilities. Even if done wisely, seeding an environment with microbial strains can only do so much. Like any organism, mycorrhizal fungi must be provided with the conditions to thrive. The soil’s microbial communities live in a state of ongoing assembly and won’t hold together for long in the face of continued disruption. For microbial interventions to be effective, more profound changes to agricultural practices are required, analogous to the changes in diet or lifestyle we might make in an effort to restore health to damaged gut flora.
Other researchers are approaching the problem from a different angle. If humans have unthinkingly bred varieties of crops that form dysfunctional symbioses with fungi, surely we can turn around and breed crops that make high-functioning symbiotic partners. Field is taking this approach, and hopes to develop more cooperative plant varieties, “a new generation of super crops that can form amazing associations with fungi.” Kiers, too, is interested in these possibilities but looks at the question from the fungal point of view. Rather than breed more cooperative plants, she is working on breeding fungi that behave more altruistically: strains that hoard less, and possibly even put the needs of plants above their own.
IN 1940, HOWARD professed that we lacked a “complete scientific explanation” of mycorrhizal relationships. Scientific explanations remain far from complete, but prospects for working with mycorrhizal fungi to transform agriculture and forestry and to restore barren environments have only increased as environmental crises have worsened. Mycorrhizal relationships evolved to deal with the challenges of a desolate and windswept world in the earliest days of life on land. Together, they evolved a form of agriculture, although it is not possible to say whether plants learned to farm fungi, or fungi learned to farm plants. Either way, we’re faced with the challenge of altering our behavior so that plants and fungi might better cultivate one another.
It’s unlikely we’ll get far unless we question some of our categories. The view of plants as autonomous individuals with neat borders is causing destruction. “Consider a blind man with a stick,” wrote the theorist Gregory Bateson. “Where does the blind man’s self begin? At the tip of the stick? At the handle of the stick? Or at some point halfway up the stick?” The philosopher Maurice Merleau-Ponty employed a similar thought experiment nearly thirty years earlier. He concluded that a person’s stick was no longer just an object. The stick extends their senses and becomes part of their sensory apparatus, a prosthetic organ of their body. Where the person’s self begins and ends is not as straightforward a question as it might seem at first glance. Mycorrhizal relationships challenge us with a similar question. Can we think about a plant without also thinking about the mycorrhizal networks that lace outward—extravagantly—from its roots into the soil? If we follow the tangled sprawl of mycelium that emanates from its roots, then where do we stop? Do we think about the bacteria that surf through the soil along the slimy film that coats roots and fungal hyphae? Do we think about the neighboring fungal networks that fuse with those of our plant? And—perhaps most perplexing of all—do we think about the other plants whose roots share the very same fungal network?