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Title: Cross-kingdom comparative genomics reveal the metabolic potential of fungi for lignin turnover in deadwood

Journal Article · · Nature Ecology and Evolution
 [1];  [2];  [1];  [3]; ORCiD logo [4]; ORCiD logo [1]
  1. National Renewable Energy Laboratory (NREL), Golden, CO (United States)
  2. National Renewable Energy Laboratory (NREL), Golden, CO (United States); Agency for Science, Technology and Research (A*STAR) (Singapore)
  3. Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
  4. Consejo Superior de Investigaciones Cientificas (CSIC), Madrid (Spain). Centro de Investigaciones Biológicas Margarita Salas (CIB)

Deadwood is a major carbon source in forests, and yet the fate of this carbon remains a gap in our understanding of global carbon cycling. Lignin, the most recalcitrant biopolymer in wood, is mainly decayed through extracellular enzymatic and chemical processes initiated by white-rot fungi. However, the intracellular conversion of lignin decay products has been overlooked in the fungal kingdom. Here we integrate comparative genomic and phylogenetic analyses to understand the distribution and evolution of enzymes responsible for modifying lignin-related aromatic compounds-such as decarboxylases, hydroxylases, dioxygenases and other downstream ring-cleavage enzymes-that funnel carbon to central metabolism across the bacterial and the fungal kingdoms. We demonstrate that specific fungal lineages conserve these enzyme families, and that the abilities to enzymatically depolymerize lignin and catabolize lignin-related aromatic compounds are not necessarily coupled. Our analyses also reveal an expanded substrate specificity of aromatic ring-cleavage enzymes during fungal evolution, as well as a clade of extracellular enzymes among them, broadening the spatial range of these biochemical capabilities. Together, our results highlight a large diversity of fungal enzymes and hosts that warrant further investigation for inclusion into carbon cycling models and biotechnological applications for the conversion of aromatic compounds.

Research Organization:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-76RL01830; AC36-08GO28308
OSTI ID:
2574775
Report Number(s):
NREL/JA--2800-93659; PNNL-SA--212707
Journal Information:
Nature Ecology and Evolution, Journal Name: Nature Ecology and Evolution Journal Issue: 9 Vol. 9; ISSN 2397-334X
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (70)

Polyphenol Oxidase Activity on Guaiacyl and Syringyl Lignin Units journal October 2024
Soil carbon sequestration journal December 2006
Early-diverging fungal phyla: taxonomy, species concept, ecology, distribution, anthropogenic impact, and novel phylogenetic proposals journal July 2021
Carbon Cycling and Formation of Soil Organic Matter book January 2007
Unconventional lignin monomers—Extension of the lignin paradigm book March 2022
A comparison between the homocyclic aromatic metabolic pathways from plant-derived compounds by bacteria and fungi journal November 2019
Biochemical and structural characterization of enzymes in the 4-hydroxybenzoate catabolic pathway of lignin-degrading white-rot fungi journal December 2024
Opportunities and challenges in biological lignin valorization journal December 2016
Wood decay under the microscope journal November 2007
Evolution of novel wood decay mechanisms in Agaricales revealed by the genome sequences of Fistulina hepatica and Cylindrobasidium torrendii journal March 2015
PAD1 and FDC1 are essential for the decarboxylation of phenylacrylic acids in Saccharomyces cerevisiae journal June 2010
Plant betalains: Chemistry and biochemistry journal September 2015
Estimating the size of the bacterial pan-genome journal March 2009
Production of β-ketoadipic acid from glucose in Pseudomonas putida KT2440 for use in performance-advantaged nylons journal April 2022
Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin journal March 2015
Discovery of Novel p -Hydroxybenzoate- m -hydroxylase, Protocatechuate 3,4 Ring-Cleavage Dioxygenase, and Hydroxyquinol 1,2 Ring-Cleavage Dioxygenase from the Filamentous Fungus Aspergillus niger journal November 2019
Structural Motifs of Wheat Straw Lignin Differ in Susceptibility to Degradation by the White-Rot Fungus Ceriporiopsis subvermispora journal November 2019
Atmospheric carbon dioxide and the ocean journal September 1993
Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists journal February 2015
Microbial degradation of aromatic compounds — from one strategy to four journal October 2011
A promiscuous cytochrome P450 aromatic O-demethylase for lignin bioconversion journal June 2018
The contribution of insects to global forest deadwood decomposition journal September 2021
SignalP 5.0 improves signal peptide predictions using deep neural networks journal February 2019
Genome sequencing of Rigidoporus microporus provides insights on genes important for wood decay, latex tolerance and interspecific fungal interactions journal March 2020
Critical enzyme reactions in aromatic catabolism for microbial lignin conversion journal February 2022
State-specific protein–ligand complex structure prediction with a multiscale deep generative model journal February 2024
Pathways for degradation of lignin in bacteria and fungi journal January 2011
Salicylic acid mediates the reduced growth of lignin down-regulated plants journal November 2011
Completion of the core  -oxidative pathway of benzoic acid biosynthesis in plants journal September 2012
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi journal June 2014
Peroxidase evolution in white-rot fungi follows wood lignin evolution in plants journal August 2019
A trait-based understanding of wood decomposition by fungi journal May 2020
Intracellular pathways for lignin catabolism in white-rot fungi journal February 2021
Fusion of Dioxygenase and Lignin-binding Domains in a Novel Secreted Enzyme from Cellulolytic Streptomyces sp. SirexAA-E journal May 2013
The Ins and Outs of Ring-Cleaving Dioxygenases journal January 2006
Analysis of Character Correlations Among Wood Decay Mechanisms, Mating Systems, and Substrate Ranges in Homobasidiomycetes journal March 2001
Recent developments in the MAFFT multiple sequence alignment program journal March 2008
InterProScan 5: genome-scale protein function classification journal January 2014
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Metabolic gene clusters encoding the enzymes of two branches of the 3-oxoadipate pathway in the pathogenic yeast Candida albicans journal March 2015
Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity journal November 2020
Estimating Gene Gain and Loss Rates in the Presence of Error in Genome Assembly and Annotation Using CAFE 3 journal May 2013
Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities journal December 2015
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms journal May 2018
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
IMG 4 version of the integrated microbial genomes comparative analysis system journal October 2013
eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences journal November 2015
InterPro in 2019: improving coverage, classification and access to protein sequence annotations journal November 2018
Selection of Conserved Blocks from Multiple Alignments for Their Use in Phylogenetic Analysis journal April 2000
Gene family expansions and transcriptome signatures uncover fungal adaptations to wood decay journal February 2021
Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics journal November 2017
phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package journal December 2011
From 13 C-lignin to 13 C-mycelium: Agaricus bisporus uses polymeric lignin as a carbon source journal April 2024
A Large and Persistent Carbon Sink in the World's Forests journal July 2011
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes journal June 2012
Lignin Valorization: Improving Lignin Processing in the Biorefinery journal May 2014
Four Aromatic Intradiol Ring Cleavage Dioxygenases from Aspergillus niger journal December 2019
Characterization of the hca Cluster Encoding the Dioxygenolytic Pathway for Initial Catabolism of 3-Phenylpropionic Acid in Escherichia coliK-12 journal June 1998
Identification and characterization of methoxy- and dimethoxyhydroquinone 1,2-dioxygenase from Phanerochaete chrysosporium journal February 2024
Manganese-Mediated Lignin Degradation by Pleurotus pulmonarius. journal January 1996
Evolutionary relationships among extradiol dioxygenases journal October 1996
Lignin Biosynthesis journal June 2003
The β-Ketoadipate Pathway And The Biology Of Self-Identity journal October 1996
Delignification by Wood-Decay Fungi journal September 1991
Vanillic acid and methoxyhydroquinone production from guaiacyl units and related aromatic compounds using Aspergillus niger cell factories journal August 2021
A secretomic view of woody and nonwoody lignocellulose degradation by Pleurotus ostreatus journal February 2016
Comparing Ligninolytic Capabilities of Bacterial and Fungal Dye-Decolorizing Peroxidases and Class-II Peroxidase-Catalases journal March 2021
A Multiomic Approach to Understand How Pleurotus eryngii Transforms Non-Woody Lignocellulosic Material journal May 2021
EvanKomp/NeuralPlexer: Used in publication software June 2025
Cross-kingdom comparative genomics and phylogenetics of aromatic catabolic enzymes in bacteria and fungi preprint May 2025