Basidiomycota Fungi and ROS: Genomic Perspective on Key Enzymes Involved in Generation and Mitigation of Reactive Oxygen Species

Abstract

Our review includes a genomic survey of a multitude of reactive oxygen species (ROS) related intra- and extracellular enzymes and proteins among fungi of Basidiomycota, following their taxonomic classification within the systematic classes and orders, and focusing on different fungal lifestyles (saprobic, symbiotic, pathogenic). Intra- and extracellular ROS metabolism-involved enzymes (49 different protein families, summing 4170 protein models) were searched as protein encoding genes among 63 genomes selected according to current taxonomy. Extracellular and intracellular ROS metabolism and mechanisms in Basidiomycota are illustrated in detail. In brief, it may be concluded that differences between the set of extracellular enzymes activated by ROS, especially by H₂O₂, and involved in generation of H₂O₂, follow the differences in fungal lifestyles. The wood and plant biomass degrading white-rot fungi and the litter-decomposing species of Agaricomycetes contain the highest counts for genes encoding various extracellular peroxidases, mono- and peroxygenases, and oxidases. These findings further confirm the necessity of the multigene families of various extracellular oxidoreductases for efficient and complete degradation of wood lignocelluloses by fungi. High variations in the sizes of the extracellular ROS-involved gene families were found, however, among species with mycorrhizal symbiotic lifestyle. In addition, there are some differences among the sets of intracellular thiol-mediation involving proteins, and existence of enzyme mechanisms for quenching of intracellular H₂O₂ and ROS. In animal- and plant-pathogenic species, extracellular ROS enzymes are absent or rare. In these fungi, intracellular peroxidases are seemingly in minor role than in the independent saprobic, filamentous species of Basidiomycota. Noteworthy is that our genomic survey and review of the literature point to that there are differences both in generation of extracellular ROS as well as in mechanisms of response to oxidative stress and mitigation of ROS between fungi of Basidiomycota and Ascomycota.

Keywords: Basidiomycota; CAZy AA auxiliary enzymes; GMC oxidoreductases; NADPH oxidase (NOX); catalase (CAT); reactive oxygen species (ROS); superoxide dismutase; thioredoxin (TRX) family proteins.

Figure 1

Extracellular ROS formation in fungi of Basidiomycota illustrating reactions and enzymes involved. For clarity, stoichiometry is not included in the catalytic reactions. Boxed enzymes are discussed in the text.

Figure 2

ROS enzymes in Basidiomycota according to taxonomy. (A) Extracellular enzyme, (B) intracellular enzyme and protein encoding genes involved in ROS generation, utilization or quenching reactions. Fungal lifestyles are depicted in different colors (legend on the top right corner). Counts represent protein models in each genome available at JGI MycoCosm (Supplementary Table 1). Genome & species coding: opened in Supplementary Table 2.

Figure 3

Intracellular mechanisms involved in generation and mitigation of oxidative stress created by ROS and RNS. Oxidized compounds, radicals and proteins are indicated in red. L• = Lipid radical, LOO• = Lipid peroxyl radical, LOOH = lipid hydroperoxide. Mechanisms that increase oxidative stress are boxed and highlighted with orange. Mechanisms that decrease oxidative stress are pointed out in green boxes.

Figure 4

Extracellular ROS generation and utilization-related enzymes in the Basidiomycota (A) in relation to their lifestyle and order-level taxonomy studied by principal component analysis on gene counts per each genome (top), and (B) distribution of genes in each species according to enzyme function and protein family (below). Ecological lifestyle groups: PAT, pathogenic; SYM, symbiotic mycorrhizal; UNDEF, saprobic undefined decomposition type; LD, litter-decomposing; OTHER, other type of wood decay; BR, brown rot; WR, white rot. Protein abbreviations are opened in the text.