Soil’s Microbial Market Shows the Ruthless Side of Forests
In the “underground economy” for soil nutrients, fungi strike hard
bargains and punish plants that won’t meet their price.
August 27, 2019
Beneath the green vegetable world we see is a dark microbial world
we don’t. The crops we eat, the forests that sustain us and most other life
forms, even the regulation of Earth’s climate — all benefit from a shadowy
network of fungi and bacteria that mobilize soil nutrients and trade them with
plants for sugars and fats. And yet the workings of this subterranean society
are almost unknown to scientists. For example, researchers just mapped for the
first time the global distribution of three major groups of these
microbes. Even in 2019, what lies beneath our feet remains a true scientific
frontier.
Despite this epistemological murkiness, public interest in the
underground ecosystem has exploded. TED talks and bestselling books extol the benevolent,
cooperative “wood wide web” of subsurface organisms that communicate,
share nutrients and sustain each other.
Toby
Kiers, an evolutionary biologist at VU University Amsterdam, is at the
vanguard of a new generation of scientists questioning that gauzy view. Through
innovative and groundbreaking studies, Kiers and her collaborators have
gathered evidence that plants and their fungal conspirators are not just
cooperating with each other but also engaging in a raucous and often cutthroat
marketplace ruled by supply and demand, where everyone is out to get the best
deal for themselves and their kind.
Doesn’t it strike you as odd? … This is undoubtedly the most
important network for our ecosystems, but we just don’t know anything about it.
Toby Kiers, VU University Amsterdam
Key to this picture is the revelation that the unseen underground
world is just as complex, sophisticated and purposeful as the visible
aboveground world we inhabit. Microbes are not simple, passive accessories to
plants, but dynamic, powerful actors in their own right. Fungi can hoard
nutrients, they can reward plants that are generous with their carbon reserves
and punish ones that are stingy, and they can deftly move and trade resources
to get the best “deal” for themselves in exchange.
Those are probably just the beginning of their talents. In a paperpublished
in June, Kiers and her colleagues pioneered a method to illuminate the fungal
marketplace in action — to make the invisible visible. The tantalizing research
hints at a capability that has been suspected but never proved: that fungi
might not be just nutrient traders but also sophisticated information
processors.
Kiers is the first to admit that scientists have far to go in
puzzling out the hidden rules of the tiny networked organisms that somehow
support all the rest of us. “Doesn’t it strike you as odd?” she said. “We know
so much about other types of networks. This is undoubtedly the most important
network for our ecosystems, but we just don’t know anything about it. … It’s
radically under-studied.”
Ancient Partners
When plants crept onto land some 500 million years ago, microbes
were waiting. Fungi and bacteria struck up relationships with their new
neighbors. Plants, after all, could do something most microbes could not:
harness solar energy to split apart atmospheric carbon dioxide and construct
energy-rich sugars and fats from the pieces. The microbes, in turn, had
mastered the art of freeing up the nutrients that plants needed from the soil —
phosphorus especially, but also nitrogen; there is evidence that microbes help
plants gain access to water as well. Some 80 percent or more of today’s land
plants form partnerships with fungi; still other plants partner with bacteria.
If the soil were somehow purged of its microbes, the plant and animal worlds
would take a big hit. The views of the great naturalist E.O.
Wilson notwithstanding, it’s microbes, not insects, that run the world.
And yet the soil microbiome is little known and even less
appreciated. There are reasons for this: Soil is opaque and microbes are, well,
microscopic. They’re also hard to study; many won’t grow in the lab, and the
wispy fungal networks that pervade soil break easily when extracted. Most of
all, though, microbes confound our understanding of life, which has been shaped
by our experience of the aboveground world. Some fungi don’t have proper cells,
for example: Their DNA-containing nuclei float through threadlike
subterranean networks that can be kilometers long. It’s often hard to say what
it means for fungi to have sex, or even to define what constitutes an
individual.
Kiers saw instead a world ordered by individual interests, where
potential cheaters lurked everywhere and species needed complex strategies to
keep their trading partners in line.
As scientists began to appreciate the importance of microbe-plant
partnerships, at least in outline, many came to see the natural world as a
cooperative, even communitarian kind of place. In the 1970s, the
microbiologist Lynn Margulis and the chemist James Lovelock developed the Gaia hypothesis, which
posits that Earth’s biosphere is, in some sense, a unified self-regulating
organism. The existence of mutually beneficial inter-species and even
inter-kingdom relationships fit right into this picture.
In the mid-1990s, a young biologist named Suzanne
Simard, now at the University of British Columbia, decided to test this
concept in a forest. “Some people thought I was crazy,” Simard (who did not
respond to multiple interview requests) said in a 2016 TED talk. For her doctoral project at Oregon State
University, she took carbon dioxide with radioactive carbon isotopes and
injected it into bags installed around pint-size birch trees growing near
Douglas fir seedlings. After a little while, she ran a Geiger counter along the
Douglas fir trees, and the device beeped like crazy. Moreover, she found that
the radioactive carbon could also flow from the Douglas firs to the birches if
she planted the bags near the firs. She had discovered that the trees shared
carbon via underground networks. Her findings, published in Nature in
1997, lit a fire under scientists and the public alike.
In describing what she found, Simard has emphasized the cooperation
she views as inherent in nature. “A forest is a cooperative system, and if it
were all about competition, then it would be a much simpler place,” she said to Yale Environment 360 in 2016. “Why would
a forest be so diverse? Why would it be so dynamic?” In her TED talk, Simard
referred to forests as “supercooperators” and made the bold assertion that
trees don’t just cooperate but communicate. She described birches and Douglas
firs as engaging in a “lively two-way conversation” mediated by their
underground collaborators. “I had found solid evidence of this massive
belowground communications network,” she said, adding later in the talk,
“Through back and forth conversations, they increase the resilience of the
whole community.”
Suzanne Simard, professor of forest ecology at the University of
British Columbia, drew researchers’ attention to the evidence that diverse
forest plants don’t just cooperate but communicate with one another.
Not long after Simard bagged saplings in the misty Pacific
Northwest, Kiers decamped from Bowdoin College in frigid Maine to the warm and
humid Barro Colorado Island in Panama. She had become fascinated by the
underground world, and, at her undergraduate mentor’s suggestion, she spent a
year at the Smithsonian’s renowned tropical field station in the main channel
of the Panama Canal, studying how soil fungi help tropical trees grow. She then
finished up her bachelor’s degree and headed to the University of California,
Davis. There she began studying one of the world’s most famous mutualisms, the
one between plants in the legume family — which includes important crops like
soybeans and alfalfa and trees like the locust — and rhizobial bacteria. These
specialized microbes nestle into spherical white nodules on plants’ roots and
become nutrient factories, converting inorganic nitrogen from the air into
biologically useful forms. They then trade the nitrogen to plants for
carbon-rich sugars.
It seems like a balanced, helpful exchange between friendly
partners. But to Kiers, the benevolent, cooperation-focused view promoted by
thinkers like Margulis and Simard was suspect. Kiers saw instead a world
ordered by individual interests, where potential cheaters lurked everywhere and
species needed complex strategies to keep their trading partners in line.
“I had this realization … that I’m less interested in cooperation
and I’m actually much more interested in the tension,” Kiers said. “I think
there’s an underappreciation of how tension drives innovation. Cooperation to
me suggests a stasis.”
As she soon learned, the legume-bacteria interaction is not so
simple. A single legume plant can host 10 or more strains of bacteria. To
Kiers, this evoked a concept from the ecologist Garrett Hardin, whose famous 1968 essay in Science, “The Tragedy
of the Commons,” argued that individuals pursuing their own interests can
destroy a common environment or resource. The legume plant itself could be seen
as a commons, and any given bacterial strain could hoard nitrogen while
continuing to feast on the plant’s sugars. “Why should they fix nitrogen —
what’s in it for them?” asked Ford Denison,
Kiers’ adviser, now an adjunct professor who runs an ecology and evolution lab
at the University of Minnesota.
Along with Stuart
West, an evolutionary theorist at the University of Oxford whom Kiers had
met in Panama, she and Denison modeled the legume-rhizobia interaction
mathematically, showing that if bacteria could “cheat” their plant hosts, the
relationship would fall apart as more and more strains defected. Kiers, Denison
and their colleague Robert Rousseau then designed an experiment that would
essentially force some of the bacteria to cheat.
Toby Kiers, an evolutionary biologist at VU University Amsterdam,
finds that the interactions among plants and their fungal symbiotes resemble a
cutthroat marketplace in which the species negotiate their exchanges of
nutrients ruthlessly.
Kiers surrounded some nodules on soybean plants with an almost
nitrogen-free air supply, making the bacteria in those nodules useless to the
plant. She found that the plant reacted by shutting off the supply of oxygen to
those bacteria, drastically reducing their reproduction. It seemed the
relationship between the bacteria and the soybeans, far from being a happy
friendship, was an uneasy détente, with the plant imposing crippling sanctions
on any bacterial partners that failed to earn their keep. The paper, which
was published
in Nature before Kiers even received her doctorate, made a huge
splash. “It’s the most cited paper in my career,” Denison said.
Kiers then switched from bacteria to fungi. While bacteria might
nestle into the roots of select groups of plants, fungi are without question
the masters of the underground domain. Certain fungi spread through vast areas
and commingle with just about every plant they encounter, even sending thready
tendrils known as hyphae directly into plants’ roots. (The name for these fungi
— “mycorrhizae” — literally fuses the Latin myco-, meaning “of fungi,”
with the Greek rhiza, or “root.”) Indeed, the mycorrhizal world forms a
sort of inversion of the vegetable one, with branching fungal networks
extending downward, mirroring the branching stems and limbs of the plants
reaching skyward.
But what really distinguishes the fungal world is its diversity and
complexity. A spoonful of soil contains more microbial individuals than there
are humans on Earth. “It’s the most species-dense habitat we have,” said Edith Hammer,
a soil ecologist at Lund University in Sweden. A single plant might be swapping
molecules with dozens of fungi — each of which might in turn be
canoodling with an equal number of plants. It’s a promiscuous party down there.
Faced with such overwhelming complexity, scientists must simplify,
just not too much (as Einstein is alleged
to have said). Kiers and her colleagues did this with a petri dish divided
into three equal-size compartments, like a Mercedes symbol. In one, they grew
carrot roots deprived of leaves along with fungal species known to associate
with carrots. The fungal hyphae, but not the plant roots, were able to grow
into the other two compartments to look for nutrients. The researchers gave a
special “heavy” form of carbon (the isotope carbon-14) to the carrots; they
also made phosphorus available to the fungi that reached into one of the other
two compartments. In this way, the scientists could track the movement of
sugars and nutrients through the simplified ecosystem. After some time, they
measured the fungi’s growth and found that the fungi with phosphorus to trade
received much more carbon from the plants.
By growing carrot roots and fungi in segmented petri dishes that
held unequally distributed nutrient resources, Kiers and her colleagues demonstrated that
the organisms favor symbiotic partners that have more to offer in nutrient
exchanges.
What Kiers’ team did next was the real coup. They inverted the
setup: carrot roots with fungi in two compartments and one compartment that
only the fungus could reach. They gave one carrot compartment more sugar than
the other. They waited, and then measured. The plant with more sugar to trade
had received far more fungal phosphorus (which in this experiment was
recognizable as the “heavy” isotope phosphorus-32).
In 2011, Kiers’
team reported in Science that not only can plants reward
high-performing fungal partners and punish poor performers, fungi apparently do
the same.
Around the same time, Hammer
reported evidence from experiments that fungi have a second trick:
They can store nutrients when a plant isn’t paying well, withholding them until
they get a better offer.
Together, the results turned scientists’ understanding of the
plant-fungal relationship on its head. No longer could mycorrhizal fungi be
seen as servants or passive accessories to their plant masters. Rather, life
forms below the surface control their own fate, just as much as those above.
It’s a dynamic marriage of equals.
“I don’t know if we should say that we enlightened the field, but I
think a lot of people thought [fungi] were much simpler” and mostly only
responded to plants’ signals, Hammer said.
The findings also established Kiers as an important thinker in her
own right. “It’s pretty amazing that this one person provided the first solid
evidence for sanctions or discrimination in what are arguably the two most
important symbioses — the legume-rhizobia system and the mycorrhizae,” Denison
said.
She followed up the lab experiment with a less
artificial one: She grew plants connected to mycorrhizae in shade and in
full sunlight. She found that the shaded plants, which photosynthesized less
and thus had fewer sugars to share, received less phosphorus from their
underground fungal counterparts.
She also began developing an economic framework for thinking about
relationships between plants and fungi. Based on observations of the
free-market system, Kiers suspects that what has stabilized plant-fungal
mutualisms for at least 470 million years is not that individual organisms are
committed to the good of the community, but rather that, in most cases, both
plants and fungi benefit more from trading with each other than from keeping
resources to themselves.
Economics provides “this huge body of literature we can borrow from
that’s actually mathematical and predictable,” Kiers said. “It can be used as a
tool to test some of these ideas.” For example, Kiers and her colleagues found
that mutualisms sometimes break down when plants find another way to get the
nutrients they need — by turning carnivorous and catching insects, for example.
They published
their findings last year in the Proceedings of the National
Academy of Sciences.
Not everyone is convinced that the cutthroat economic world of
markets and traders describes plants and microbes well. “I think it’s possible
that sometimes the fitness interests of partners just happen to be really well
aligned,” said Megan Frederickson, a professor of ecology and evolutionary
biology at the University of Toronto who has argued in several papers that cheating is far less
common in nature than Kiers believes. “I think some other people take
the view that it’s probably impossible for two partners in any interaction to
have perfectly aligned interests.”
That view has also come to dominate the popular literature. In
2016, the German forester Peter
Wohlleben, drawing heavily on Simard and a few other scientists,
published The Hidden Life of Trees. The book became an international
bestseller. Wohlleben, a strong advocate for a communitarian view of nature,
wholeheartedly promoted fungi’s supposed beneficence and cooperative nature,
writing, “The fungi that populate [trees’ roots] seem to be intent on
compromise.”
Together, the results turned scientists’ understanding of the
plant-fungal relationship on its head. No longer could mycorrhizal fungi be
seen as servants or passive accessories to their plant masters.
Kiers, characteristically, has turned to different sources for
inspiration. A few years ago, she read the economist Thomas Piketty’s Capital
in the Twenty-First Century, which emphasizes the role of resource
inequality in shaping human societies. Kiers suspected that introducing
inequality into her fungus-plant ecosystem would reveal novel insights. But she
found herself facing the same challenge that had stymied so many scientists:
She had no way to directly see what fungi were doing. She had gotten a lot of
mileage out of measuring nutrients going in and seeing where they ended up, but
what happened within the fungi themselves remained a black box.
“That’s how we start lab meeting every week: ‘If we can’t talk to
them, how do we get at that question?’” Kiers said.
The breakthrough came unexpectedly. Kiers had gotten a Dutch
government grant to work with an artist on a stop-motion video depicting
phosphorus and other nutrients moving through the fungal network, using LEDs to
represent nutrients. She showed the animation at a 2014 scientific conference.
“Wouldn’t it be cool if we could do that?” she asked her audience.
Matthew Whiteside, a chemist then working at the University
of British Columbia, approached Kiers afterward. “We really can do that,” he
said.
Whiteside — who, incidentally, had known Margulis as a family
friend and spoken with her about pursuing science — had developed a way to tag
biomolecules with quantum dots, nanometer-scale bits of semiconductor that
absorb certain short wavelengths of light (usually ultraviolet) and re-emit
light, or “fluoresce,” at longer wavelengths. Kiers hired him. The two spent
several years developing the technique and ensuring that they could distinguish
the dots’ emissions from the plant cells’ natural fluorescence. They also had
to ensure that the dots wouldn’t poison fungi or plants.
In this micrograph of fungal hyphae, nutrient biomolecules
containing phosphorus have been tagged with quantum dots, which fluoresce as
green. This labeling technique allowed Kiers’ team to capture photographically
what had only been imagined in their video animation.
Victor Caldas
Kiers and Whiteside then set up another experiment in the
three-compartment petri dish. They grew carrot roots with fungi in one
compartment and allowed the fungi to expand into the other two. Then they
introduced apatite, a phosphorus-containing mineral, into the fungi-only
compartments. In one, they labeled the apatite with a red-fluorescing quantum
dot; in the other they used a blue dot. They used specialized microscopes to
quantify the emitted light.
At first they gave each fungal compartment equal amounts of
apatite. As expected, the fungi took up the phosphorus-laden compound through
their networks but didn’t grow much, choosing instead to store much of the
nutrient rather than trade it.
Then came the part inspired by Piketty’s work on economics. Kiers
and Whiteside added more phosphorus to one compartment than the other, setting
up resource inequalities, with one fungal group controlling up to 90% of the
element. The fungi responded by trading with the plants far more than when
phosphorus was evenly distributed in the environment.
Most impressively, the fungi moved nutrients from the “rich” to the
“poor” region and grew faster in the poor region. Kiers’ team believes that’s
because the fungi could extract a higher “price” from the plants in the form of
carbon-rich sugars where phosphorus was scarce — though Kiers notes that they
couldn’t track the carbon directly.
We’re starting to deconstruct [the fungal network] piece by piece.
Toby Kiers, VU University Amsterdam
“This is totally opposite of what we had anticipated,” she said.
She thought trading would be highest where nutrients were already abundant.
The demonstration impressed others. “We often think of fungi or
other microbes as not particularly intelligent,” said Kabir
Peay, a biologist at Stanford University. “This study goes to show that
across these networks, one of the reasons they can be so successful is that
they can make what seem to be fairly sophisticated decisions about where to
allocate resources to optimize the return they get.”
But scientists must take care when applying market concepts to the
biological word, noted Ronald Noë, a biologist and professor emeritus at the
University of Strasbourg in France who helped pioneer biological market theory
in studies of primates, and who assisted Kiers’ team with the economic
analysis. “What they describe is a mechanism by which you could be a trader in
the market — you can see how they could do it. But they didn’t actually prove
that they did it,” Noë said. “If there would be a market, the fungus would
bring its nutrients from one plant to the other. But in the experiment, there’s
only one plant. The fungus is not choosing.”
The experiment revealed a second surprise. Phosphorus did not
just flow from the rich region to the poor one. Kiers and Whiteside caught some
of the glowing nutrients oscillating back and forth through the network every
five minutes in a regular rhythm.
The scientists don’t know what these oscillations mean. But they do
know that oscillations are common ways to encode information. For example,
radios work by encoding information in oscillations of radio waves, which are
low-frequency electromagnetic waves. Could the fungal oscillations be a form of
information transfer across the network?
There is, in fact, strong evidence that information flows across
fungal networks. In 2013, David
Johnson, a biologist then at the University of Aberdeen in Scotland,
discovered that bean plants attacked by aphids sent chemicals underground
through fungal networks and into nearby plants that were then alerted to the
presence of the pests. Simard has found similar chemical releases in the
forests she studies.
But in those studies, scientists inferred what was happening
underground from measurements of chemicals in trees. Left unanswered was
whether fungal networks are merely conduits of plant-to-plant signals, or if
they can process the information they receive. If someone were able to prove
the latter, said Erik
Verbruggen, a biologist at the University of Antwerp in Belgium who did his
doctorate with Kiers, “that would be quite extraordinary.”
Kiers has illuminated the fungal network for the first time. Her
next goal is to narrow the gulf between her experimental setups and the
complexity of nature. For example, Kiers’ petri dishes flatten the plant-fungus
world into two dimensions, but in real soils, fungal networks are 3D. Different
species’ networks overlap and interweave, making the wood wide web more like a
wood wide tangle with dozens of independent wiring schemes.
“I’d be the first to admit that this is incredibly artificial,”
Kiers said of her lab setup. “But that’s actually the beauty of it. We’re
starting to deconstruct [the fungal network] piece by piece.”
Kiers is now teaming up with the fluid dynamics researcher Howard
Stone of Princeton University, the biophysicist Tom Shimizu of VU
University, and the network ecologist Hirokazu Toju of
Kyoto University. (Their work is funded by a grant from the Human Frontier Science Program to
encourage international collaborations on high-risk projects.) They plan to use
microfluidic tools to create intricate 3D environments that more closely
resemble real-world fungal networks. Stone hopes to augment Kiers’ quantum-dot
tags with other techniques for tracking resources such as the carbon that
plants trade; some commentators critiqued Kiers’ inequality study for failing
to account for that carbon.
“There’s a whole system that we have to set up, including imaging
and understanding and possibly modeling, that no one’s done,” Stone said.
For Kiers, the collaboration promises further revelations about how
much we’ve misjudged our microbial counterparts.
“Even I, still to this day, underestimate fungi,” she said.