Video: How fungus invades and digests fruit
Single combat, assassination, chemical warfare, even mind control: the Geneva conventions don’t apply when fungi go to war
TO CRUNCH your way across a meadow or through a wood on a crisp winter’s day is to traverse a battlefield. That rural tranquillity is a mere veneer. Beneath the soil, in those piles of falling leaves or that moss-covered tree stump, war is being waged.
You might see the standards of some of the troops standing proudly above the surface: perhaps a field mushroom, or a bracket fungus. The passivity is deceptive. Out of sight, scenes of peculiar barbarism and brutality are being played out. One-on-one combat, stealth assassination, chemical warfare, even mind control: when mushrooms get martial, the Geneva conventions most definitely do not apply. You may find some of the scenes I am about to describe disturbing.
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Before we delve into gory details, however, a big word in defence of fungi. This diverse and distinct kingdom of organisms – neither plant, animal nor bacterium – is largely responsible for breaking down and recycling bulky, dead plant tissues. Fungal activity releases the nutrients locked inside material rich in lignin and cellulose, from leaves and twigs to mighty trunks, so that further generations of plants can grow.
Fungi thus ensure that land-based ecosystems thrive. They probably also created them in the first place, helping to make the first soils and assisting photosynthetic organisms in colonising the land. One particular group, the mycorrhizal fungi, feed nutrients and water directly into plant roots, and are paid for this service with sugars from the plant. In this intimate relationship, which evolved just as life was getting a toehold on land about 450 million years ago, fungi colonise the fine roots of plants and extend into soil as long thin tubes called hyphae, the better to gobble up nutrients for both.
(Image: Brian Lightfoot/Naturepl.com)
Even if fungal ends are justified, we can still blanch at some of the means. Fungi are territorial beasts, and recognise their own. If the mycelium of any individual fungus – the mass of interconnected hyphae that forms its generally hidden body – splits into smaller networks, these happily grow independently. If they later encounter one another again, they will fuse back together to form a bigger mycelium and so pool resources.
It is another story when genetically different individuals of the same species meet: on touching, they will recoil behind the fungal equivalent of a picket fence. Actually, make that barbed wire: the dense, contorted, much branched walls of hyphae that fungi build to mark out their territory are not designed to invite friendly interaction. These impenetrable barriers are the lines, black or autumnal brown and orange, that mark out spalted wood used to make decorative bowls and jugs.
But woe betide a mycelium encountering a different species of fungus – and as there are thousands of species in a typical woodland landscape, it happens often. This is when the battle lines are truly drawn.
For some fungi, war means bare-hand killing. Soil-dwelling fungi of the genus Trichoderma, for instance, coil around a victim’s hyphae and use mechanical force and enzymes to penetrate it, sucking out food.
But mostly the means are more insidious (see “Fungal fighters: Cruel weapons of the forest floor“). We are familiar with some of the volatile chemicals that fungi produce, such as the odour of cooking mushrooms or the smell of rot. When fungal species encounter each other, chemical warfare often ensues. Some, such as the versatile assassin the sulphur tuft, produce agents such as sesquiterpenes that are as damaging to fungi as nerve gas is to humans, and quinolinium compounds like those used in commercial fungicides. The ubiquitous turkey tail fungus, on the other hand, is a poisoner. It secretes enzymes into the food sources on which the opponent fungus feeds, killing and dissolving the other combatant from inside, so its territory and food can be taken as spoils of war – assuming it avoids its own predators.
What unites fungal fighters is that they are bullies. Given a choice of several opponents, an aggressor will attack the weakest first, going for others only when it has consolidated its territory. Things don’t always go to plan. Thanks to an evolutionary arms race that has been escalating for millions of years, the aggressor can often get as good as it gives. The chemical fallout from two evenly matched species can create a no man’s land no party can occupy.
While there is a natural hierarchy of combative ability in most fungal ecosystems, with some species good in attack and others good in defence, the conditions of the battlefield – whether it is warm or dry, or the availability and quality of food – can also be decisive. The sulphur tuft wins more battles in warmer weather, for example, while Daldinia concentrica or King Alfred’s cake – named for its black fruit bodies that resemble charred bakery produce – is formidable when it is dry. Climate change might be expected to alter the outcomes of these hidden battles. Bystanders can influence the outcome too, by emitting some of their chemical arsenal or through skirmishes against a main contender.
If you look carefully, evidence of these epic battles abounds in the woods. The exploratory mycelium scouting for food and enemies is visible if you gently clear away the layer of leaves blanketing the woodland floor. Turning over a decaying log can reveal cords of hyphal aggregations, rather like the hawsers from a ship to the dockyard, creating a vast network on the forest floor. They are supply lines spreading crucial water and food around the system and to the front line: after all, an army marches on its stomach. The front lines themselves are harder to discern in the forest, but in lab cultures they are sometimes accompanied by blood red pigments, perhaps defensive chemicals, that make them look even more like human killing fields.
Fungi aren’t just aggressive to their own kind. Nematodes – minute, worm-like soil-dwelling creatures – are favoured prey forming a nutrient-rich supplement to the diet. Fungi have evolved nematode traps of varying complexity, including adhesive protrusions that emerge on the hyphal surfaces like lethal lollipops, and adhesive nets and nooses to strangle the unwary.
Equally macabre demises are brought about by fungi producing spores that stick to the outsides of nematodes, or using hooks and protrusions that lodge within the worms’ mouths. Irrespective of how the nematode has been incapacitated, the next step is the same: the fungus pushes its hyphae into the worm’s body and liquidises its body contents.
“The fungus pushes hyphae into the nematode’s body and liquidises its contents”
Insects and other arthropods aren’t safe, either. Their multilayered exoskeletons, made of waxes, lipoproteins and often anti-fungal compounds, protect their vulnerable interiors rather as an army tank protects its human cargo. But some fungi penetrate these defences and even evade haemocytes, specialised warrior cells sent out by the insect’s immune system to seek and destroy invaders. Once inside, one group of fungi, the Entomophthorales – their name means “insect destroyer” – choke their victims to death by blocking their spiracles, or breathing tubes. Killers from the Helotiales, meanwhile, spread through the body cavity in a yeast-like form, exuding deadly toxins.
Forest fronts
Not that death has to be instant: some ant-preying fungi of the genus Ophiocordyceps prefer to co-opt their victims as a zombie army first. These brain-manipulating fungi make their hosts climb plants to higher places, and then shoot their spores like bombs from an aircraft, increasing their spread. In their death throes, the ants cling to or bite twigs and leaves, anchoring the fungus in prime positions. Admittedly, your autumnal wanderings would have taken you a long way before you saw this sort of macabre spectacle: Ophiocordyceps‘s stamping ground tends to be the rainforests of the tropics.
Lest we stray too far towards portraying these particular fungi as evil geniuses, it is worth bearing in mind that altering a victim’s behaviour doesn’t always play into the perpetrator’s hands (were they to have any). Sometimes, the effect of the mind-bending spell is to make ants move like drunkards who have over-imbibed on another fungal product – alcohol. Their erratic movement and insecure footwork then fail them in their high-wire act, and they plummet to the forest floor.
There is more to studying the military tactics of mushrooms than pure voyeurism. Even in the late 19th century, the powdery spores of the white muscardine (Beauveria bassiana) and green muscardine (Metarhizium anisopliae) fungi were mass-produced in Russia and the US in an attempt to control insect species they parasitise, among them the Colorado potato beetle.
The high cost, when compared with chemical insecticides, and complications in production, storage, distribution and application, meant these initiatives met with limited success. But concerns about the environmental consequences of chemical control mean “biocontrol” is coming back into favour. With it, there is an increased interest in how fungi’s natural chemical arsenals work. Fungal insecticides have the decisive advantage that they can be selected to target specific organisms, minimising unintended harm to other species.
Fungal aggression towards microbes is the origin of our best-known antibiotic, penicillin. Molecular biology tells us that within every fungal genome there are multiple pathways for producing similar killer chemicals – yet just a few are produced when these fungi grow alone in the lab. It’s only in the heat of a fight that they turn on the production of a diverse antimicrobial arsenal. Understand what triggers this arms race, and better drugs could be within our grasp.
But how best to get there? In my research group we map out morphing mycelial networks in the forest in an attempt to better understand the rules of fungal warfare. Back in the lab we set up fungal battles in large trays of soil and blocks of wood, as if setting up games of strategy. We control climate, food and opponents, but the fungi – the “pieces” of our game – move themselves. Will they beat all-comers, or be displaced by some upstart? What weapons or tactics will they use? It is all great fun, and it is tempting to take bets on the outcome. But more importantly, it gives us a deeper insight into this often overlooked aspect of natural ecosystems like the woodlands we wander in. Through work like this we can better ensure their survival – and perhaps turn them to our advantage.
Read more: “Fungal fighters: Cruel weapons of the forest floor“
This article appeared in print under the headline “Soils of war”
