How Fungi Saved the World

A long time ago, back before the dinosaurs were even a twinkle in a primitive reptile's eye and before that reptile's ancestor was even a twinkle in a primitive amphibian's eye, before plants thought seeds were a neat idea and invertebrates were disquietingly large, terrestrial life found itself with a bit of a problem. We're in the Carboniferous period, and the world's biggest coal deposits are being laid down in the first forests. The atmosphere is much different than in modern times: carbon dioxide concentrations are approaching disastrously low levels, and oxygen is soaring. The foot-long dragonflies that flit through this dense, breathable atmosphere are having a good time, but we're on the brink of a major ice age caused by global cooling.

The culprits of this looming disaster are the last we'd suspect: trees. To understand why, we need to turn back the clock even further. Around 90 million years before the Carboniferous period and 430 million years before present, the first vascular plants emerged from early tide pools. In order to stay upright, these plants employed cellulose, a chain of simple sugars known as glucose (two glucose molecules make up sucrose, or table sugar). This was great for plants, as it was easy easy to make and offered rigid yet flexible support, but it made life difficult for decomposers, who needed an enzyme that could turn cellulose back to digestible glucose. Bacteria and fungi eventually evolved this ability, but animals never would, and they became dependent on symbioses with these simpler organisms.

A section of Lepidodendron "bark" showing the diamond-shaped leaf scars. Photo credit: State Museum of Pennsylvania. 

A section of Lepidodendron "bark" showing the diamond-shaped leaf scars. Photo credit: State Museum of Pennsylvania. 

By the dawn of the Carboniferous period, plants developed a new kind of support material, called lignin. Lignin was an improvement development over cellulose in several ways: it was harder, more rigid, and, being more complex, almost impossible to digest, which made it ideal for protecting cellulose. With lignin, plants could make wood, and it lead to the first treelike growth form. One of the early founders of these primeval forests was Lepidodendron (from the Greek lepido meaning “scale” and dendron meaning “tree,” so named for the leaf scars that resulted in a scaly trunk). Lepidodendron wasn't a true tree but a member of an early offshoot of the higher plants known as lycopods, today comprised of the much smaller club mosses and quillworts. Based on reconstructions of the fossils, it is estimated that Lepidodendron stood a stately 100 feet tall, putting it at the very top range of the early flora and head and shoulders above many trees that exist today. As the Carboniferous period continued, Lepidodendron and its cousins spanned the tropics in vast forested swamps.

Here is the crux of our problem: lignin made the lycopod trees a little too successful. Because their leaves were lofted above many herbivores and their trunks were made inedible by lignin, lycopods were virtually impervious to harm. They grew and died in vast quantities, and their trunks piled up in swamps, eventually becoming submerged and locking huge quantities of carbon dioxide out of the atmosphere for good in the form of coal. Without any decomposition to recycle this carbon, atmospheric carbon dioxide levels crashed, leading to global cooling and making it much harder for plants to grow. Atmospheric oxygen concentration, in turn, soared to an estimated 35%, much higher than the 20% of modern times.

But why was all this lignin laying around in the first place? Plenty of organisms had found a way to make use of cellulose, so why didn't they jump on this new source of energy that was laying around free for the taking? The are several reasons: first, whereas cellulose was made of glucose, which can be readily converted to energy, lignin was based on phenol, a derivative of benzene, which is only a good energy source when it's on fire. This isn't a solution for your average bacterium. Digesting lignin was so difficult that lycopods had free reign over the planet for over 40 million years, leading to the world's first and only wood pollution crisis.  Finally, however, a fungus belonging to the class Agaricomycetes – making it a distant cousin of button mushrooms – did find a crude way to break down lignin. Rather than devise an enzyme to unstitch the lignin molecule, however, it was forced to adapt a more direct strategy. Using a class of enyzmes called peroxidases, the fungus bombarded the wood with highly reactive oxygen molecules, in much the same way one might untie a knot using a flamethrower. This strategy reduced the wood to a carbohydrate-rich slurry from which the fungus could slurp up the edible cellulose.

An etching of what a Carboniferous forest may have looked like. The canopy was dominated by lycopod trees such as Lepidodendron (middle ground, left), and the understory by ferns (fore, left) and giant horestails (fore, right), and the middle layers by tree ferns (middle ground, center) and early gymnosperms. The Cordaites (behind the Lepidodendron) in this picture are distant ancestors of pine trees.

An etching of what a Carboniferous forest may have looked like. The canopy was dominated by lycopod trees such as Lepidodendron (middle ground, left), and the understory by ferns (fore, left) and giant horestails (fore, right), and the middle layers by tree ferns (middle ground, center) and early gymnosperms. The Cordaites (behind the Lepidodendron) in this picture are distant ancestors of pine trees.

The oyster mushroom (Pleurotus ostreatus) is both a white rot fungus and a versatile entree. Photo credit: Aaron Sherman.

The oyster mushroom (Pleurotus ostreatus) is both a white rot fungus and a versatile entree. Photo credit: Aaron Sherman.

This was the one and only time in the last 300 million years that the wood-rotting ability evolved. All the fungi today that can digest wood (and a few that can't) are the descendants of that enterprising fungus. Its strategy may have been inelegant, but wood decay played a crucial role in reversing the loss of carbon dioxide in the atmosphere and bringing about the end of the Carboniferous period.

What would have happened if white rot fungi had never evolved? We can only speculate, but it's possible the world of today would look a lot like the world at the end of the Carboniferous period – cooler, high in oxygen, and with a denser atmosphere. Dragonflies with foot-and-a-half wingspans might still roam the forests, but the plant life might still be primeval, stifled by the lower carbon dioxide concentrations. Many a homeowner may disagree, but we're lucky wood-rotting fungi evolved. 

Andrew Tomes is an MS student at SUNY-ESF in Syracuse whose work focuses on the mycorrhizal partners of the American chestnut. He earned his B.S. in Botany from the University of Maine, where he worked on wetland restoration. When not in the field, the lab, or the classroom, he can often be found in the kitchen baking bread.

Sources:

Floudas D, et al. Science 336: 1715-1719 (2012)

Graham BJ, et al. Nature 375: 117-120 (1995)

Robinson JM. Palaeogeography Palaeoclimatology, Palaeoecology97: 51-62 (1991)