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Functional and Systems Biology

White-rot Fungi Eat All the Components of the Wood They Decompose

White-rot fungi utilize lignin from wood as a source of carbon.

White-rot fungi are well known to break down lignin and convert it into CO<sub>2</sub> and H<sub>2</sub>O in nature. A new study reveals that these fungi incorporate lignin-breakdown products into their central metabolism. Davinia Salvachúa Rodríguez (National Renewable Energy Laboratory, Golden, CO)

White-rot fungi are well known to break down lignin and convert it into CO2 and H2O in nature. A new study reveals that these fungi incorporate lignin-breakdown products into their central metabolism. Davinia Salvachúa Rodríguez

The Science

Plant cells are enveloped in a cell wall composed mostly of cellulose and lignin. While cellulose is easily degradable, lignin is a very sturdy polymer. White-rot fungi have an extraordinary ability to break down lignin. However, scientists do not know the details of the fate of the lignin deconstruction products. To better understand this process, researchers used synthetic isotope-labeled compounds that mimic those produced by lignin breakdown and fed them to the fungi. Then, they determined which metabolites lignin was converted into by tracking the isotope-labeled compounds within the fungal cells. This study reveals that white-rot fungi uptake lignin deconstruction products and utilize them as carbon sources. Furthermore, the researchers identified a diversity of metabolites and enzymes involved in the conversion of lignin components.

The Impact

Lignin accounts for 30 percent of the organic carbon on Earth. Therefore, white-rot fungi—the most efficient lignin-degrading organisms—play a critical role in global carbon cycling. A longstanding belief was that white-rot fungi convert lignin to CO2 and H2O outside their cells to simply gain access to the plant cell wall sugars that compose cellulose. The current study overturns this decades-old dogma by demonstrating that white-rot fungi also incorporate carbon from lignin-derived compounds. Furthermore, this study establishes a foundation for employing white-rot fungi in biotechnological applications, such as lignin bioconversion into value-added products, which is a key step toward enabling a sustainable plant-based bioeconomy.

Summary

Scientists have largely overlooked the intracellular metabolization of lignin deconstruction products in white-rot fungi. This was due to the difficulty of studying these fungi in culture and to the lack of genetic tools for white-rot fungi. Scientists have now overcome these obstacles by labeling carbon atoms within synthetic aromatic compounds with a carbon isotope (13C). These synthetic compounds are identical to those that compose lignin in poplar trees. The team used these 13C-labeled chemicals as the carbon source in fungal cultures to track their utilization through the central metabolism of fungal cells. The team selected two species of white-rot fungi that use different mechanisms to degrade lignin and cellulose. Using this system, they discovered that the fungi converted the 13C-labeled aromatic compounds into amino acids, which are the main components of proteins.

Taking advantage of the availability of sequenced genomes for both fungal species, the researchers applied systems biology and computational genome analysis approaches to predict their aromatic catabolic pathways. Then they conducted metabolomic, proteomic, and transcriptomic analyses to confirm the existence of predicted catabolic intermediate metabolites as well as the enzymes that generated them. The team obtained further evidence of the metabolic roles of some of those enzymes by producing them in the laboratory bacterium Escherichia coli and then verifying that they had the predicted enzymatic activity in vitro.

Contact

Davinia Salvachúa Rodríguez
National Renewable Energy Laboratory, Golden, Colorado
davinia.salvachua@nrel.gov

Funding

This research was supported by an Early Career Research Program award to Davinia Salvachúa Rodríguez funded by the U.S. Department of Energy (DOE) Office of Science, Biological and Environmental Research program. A portion of the research was performed in the Joint Genome Institute located at Lawrence Berkeley National Laboratory and in the Environmental Molecular Sciences Laboratory located at Pacific Northwest National Laboratory. Part of this work was also supported by a Laboratory Directed Research and Development project at the National Renewable Energy Laboratory.

Publications

C. del Cerro, E. Erickson et al. “Intracellular pathways for lignin catabolism in white-rot fungi”. PNAS. 118, e2017381118 (2021). [DOI: 10.1073/pnas.2017381118]

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