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Comparative Genomic Study Explores Evolution of Wood-Degrading Fungal Enzymes

NEW YORK (GenomeWeb News) – The type of enzymes that white rot fungi use to break down a stubborn polymer called lignin in wood have been around for some 300 million years, originating in an ancestor of fungi in the Agaricomycetes class, a new study suggests.

A large international team led by investigators at Clark University and the US Department of Energy's Joint Genome Institute compared the genomes of 31 fungi, including a dozen sequenced for the study, looking at the presence or absence of genes from 27 enzyme families. The study, appearing online today in Science, offers insights into the history of peroxidase enzyme expansion in white rot fungi and the loss of these enzymes in related brown rot and mycorrhizal fungal species.

"Our study was designed to reconstruct the evolution of lignin decay mechanisms in fungi, analyze the distribution of enzymes that enable fungi to break down lignin, and better define the evolution of the gene families that encode those enzymes," co-corresponding author David Hibbett, a Clark University biologist, said in a statement.

Moreover, the researchers' catalog of lignin-degrading enzymes in the fungal genomes is expected to prove useful for biofuel studies and other applications that hinge on lignin breakdown, a process that helps in accessing the plant carbohydrate cellulose.

Finally, based on the enzymatic patterns in the fungal genomes and the estimated timing of their expansion, the team speculated that the evolution of white rot fungi — and, with it, a rise in lignin-degrading enzymes — may have cut the Carboniferous period short by making it possible to degrade the sorts of plants that would previously have been fossilized and deposited as coal.

"When you read about coal formation it's usually explained in terms of physical processes, and that the rate of coal deposition just crashed at the end of the Permo-Carboniferous," Hibbett said. "Why was that?"

"The evolution of white rot fungi could've been a factor — perhaps a major factor," he reasoned. "Once you have white rot you can break down lignin, the major precursor of coal. So the evolution of white rot is a very important event in the evolution of carbon cycle."

The study, which is part of the broader Genomic Encyclopedia of Fungi project, was supported by the National Science Foundation's Tree of Life program and its Partnerships for Enhancing Expertise in Taxonomy program.

Collaborators at JGI sequenced a dozen new fungal genomes for the effort. These included genomes for six white rot species, five species of brown rot, and one so-called mycoparasite.

In addition to doing phylogenetic analyses on these fungi and 19 other fungi sequenced previously, the team sifted through all 31 genome sequences to assess their enzyme gene family repertoires.

Amongst the lignin-degrading enzymes, for instance, researchers found that white rot fungal genomes contain between five and 26 copies of class II peroxidase enzymes. In contrast, brown rot species and the ectomycorrhizal species Laccarria bicolor were missing these enzymes.

Nevertheless, the team's evolutionary analyses indicated that ancestors of all of the Agaricomycetes, which includes brown rot and ectomycorrhizal, contained between three and 16 genes coding for lignin-zapping class II peroxidase enzymes. That suggests the enzymes were lost in some fungal lineages over time, while expanding in white rot lineages.

Moreover, the researchers' molecular clock analyses, calibrated using fungal fossil data, indicates that the advent of white rot fungi containing enzymes that could degrade lignin coincided with — and may have influenced — the end of the Carboniferous period some 290 million years ago.

"The idea that a stable (inedible) form of organic carbon can become edible (and thus more difficult to bury over time), changes our perspective not only on global energy storage in the past, but on what it means for present day carbon sequestration and storage," University of Southern California environmental sciences researcher Kenneth Nealson, who was not involved in the study, said in a statement. "[I]n that sense this idea will have a big impact on our thinking about the past and the present."

Under the DOE JGI Community Sequencing Program, researchers have embarked on a 1000 Fungal Genomes effort aimed at sequencing two fungi each from 500 fungal families over the span of five years.

"There's an estimated 1.5 million species of fungi," Oregon State University botany and plant pathology researcher Joseph Spatafora, co-author on the current study and head of the 1000 Fungal Genomes project, said in a statement. "We have names for about 100,000 species, and we're looking at 1,000 fungi in this project."

"This is still the tip of the iceberg in looking at fungal diversity," he added. "[W]e're trying to learn even more to gain a better idea of fungal metabolism and the potential to harness fungi for a number of applications, including bioenergy."

Meanwhile, a European effort called PEROXICATS plans to continue characterizing and searching for peroxidase biocatalyst enzymes that could be exploited to harvest energy from plant biomass.

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