White Rot Fungi Slowed Coal Formation

The evolution of the ability to break down a plant's protective lignin largely stopped the geologic burial of carbon that formed present-day coal deposits—and may provide secrets to making biofuels from inedible parts of plants

Courtesy of A. Justo and D. Floudas

A toughened crosshatch of carbon-based molecules is all that stands between plants and their total destruction at the hands of an array of microbes and fungi. Called lignin, the compound enables redwoods to tower and woody herbs to resist rot. As a result, lignin is the second-most abundant biological compound on the planet—and the bane of would-be biofuel-makers everywhere, blocking their best efforts to make fuels from the inedible parts of plants. It is also the reason for the vast deposits of coal laid down millions of years ago.

Now a new genomic analysis suggests why Earth significantly slowed its coal-making processes roughly 300 million years ago—mushrooms evolved the ability to break down lignin. "These white rot fungi are major decomposers of wood and the only organism that achieves substantial degradation of lignin," explains mycologist David Hibbett of Clark University in Massachusetts, who led the research published in Science on June 29.

By comparing 12 newly sequenced genomes of mushroom fungi with 19 existing genomes, the researchers determined that an ancestral white rot fungi (Agaricomycetes) first evolved the ability to break down lignin. The scientists then used so-called "molecular clock analysis"—a dating technique based on the hypothesis that genes accumulate mutations at a relatively regular rate like trees form rings that record their growth. Such an analysis suggests that an ancestral white rot fungi developed this lignin-degrading ability roughly 290 million years ago, a conclusion backed by comparison with the appearance in the fossil record of three other types of fungi (although the first definitive white rot fossil does not appear until roughly 260 million years ago) and the subsequent expansion and refinement of the arsenal of enzymes employed. The 60-million-year-long Carboniferous period—when the bulk of the world's coal deposits were laid down and atmospheric CO2 levels declined—ended roughly 300 million years ago.

The coincidental timing suggests the appearance of this ability to break down lignin helped slow the massive burial of organic carbon via nondegraded tree trunks and other wood, such as the lignin-rich fernlike plants known as arborescent lycophytes, now extinct. Previous explanations largely argued that such coal formation was a result of the Carboniferous's swampy conditions—after lignin-rich plants fell into these swamps, they simply were buried rather than broken down by fungi or microbes and turned to peat and then coal over geologic time frame. "They're not mutually exclusive," Hibbett notes, although more of the easily overlooked fungal fossils would need to be found to determine the truth.

How exactly white rot breaks down lignin remains unknown. The fungi releases reactive molecules and enzymes that seemingly tear the plant-protecting compound apart via "brute force," in the words of Hibbett. Once the protective lignin is out of the way, the white rot fungi feast on the cellulose, which comprises more digestible plant sugars. And subsequent evolution has given so-called brown rot fungi the means to work around lignin without attacking it directly. "They have evolved a way to get at cellulose and leave the lignin behind," Hibbett says, which results in the crumbly, brown logs littering temperate forests today—potentially coal in the distant future.

That puts both white rot and brown rot well ahead of human chemists, who have been trying to both eliminate lignin and degrade cellulose to make biofuels from the nonedible parts of plants. A better understanding of the enzymes involved—as well as the genes that enable the fungi's cellular machinery to make those enzymes—may help human chemists catch up, says geneticist Igor Grigoriev of the U.S. Department of Energy's Joint Genome Institute, which did much of the sequencing. The group plans to sequence yet more genomes to learn fungi's tricks as part of the 1,000 Fungal Genomes Project, although that still represents less than 0.1 percent of estimated extant fungal species. Fungi "play a huge role in the evolution of terrestrial ecosystems and the carbon cycle," Hibbett notes. "They don't get enough attention."

In the meantime, the long-running evolutionary war between woody plants and fungi continues. "We still have trees, but we don't have arborescent lycophytes. We don't know if white rot fungi caused that extinction, but it's an interesting possibility," Hibbett says. "It's an ongoing tug of war between fungi and woody plants."

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