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.

Bioremediation potential of industrial laundry effluent by agaricomycetes from brazilian tropical dry forest

“…Normally, the KM should not vary much if it was a pure enzyme, but because it is an enzymatic complex, there was a synergism between the intra and extracellular enzymes present. This synergism allowed the potentiation of the complex (Mattila et al, 2022;Bernal et al, 2021;Sakai et al, 2022), obtaining an almost complete degradation of the ICD in the concentration of 50 ppm in 25 days of experimentation, above 90% in Gi2 and above 80% in Gi1 (Table 2).…”

“…In shorter periods of growth and WAN (Gi1, 20 days), besides the production of ligninolytic enzymes due to lack of nitrogen, the amount of carbon present stimulates the fungus in the production of intermediate enzymes that degrade other recalcitrant xenobiotic compounds, such as other oxidases producing hydrogen peroxide and intermediate metabolic compounds of low molecular mass (Kaushik & Malik, 2009;Janusz et al, 2017;Mattila et al, 2022;Kenkebashvili et al, 2012;Gupta & Asim, 2019). Therefore, a carbon source mixed with the NL accelerates the bioremediation of the TE (Gupta & Asim, 2019;Davila et al, 2020;Conceição et al, 2017).…”

“…The lignin degradation occurs because of multi-enzymatic process resulting from the coordinated action of a series of intra and extracellular enzymes such as oxidoreductases, as well as other oxidases producing hydrogen peroxide and by intermediate metabolites of low molecular mass (Mattila et al, 2022;Bernal et al, 2021;Sakai et al, 2022).…”

Substrate specificity mapping of fungal CAZy AA3_2 oxidoreductases

“…The interplay of AA3_2 AADH, GDH, and laccases was also observed, and both AA3_2 AADH and GDH were found to inhibit the formation of laccase-oxidized phenolic products [ 25 , 26 ]. Moreover, a recent genetic study has revealed that large numbers of copies of AA3_2 encoding genes of Basidiomycota fungi co-occur with large numbers of copies of AA2 class II high-redox peroxidases, particularly in white rot and litter decomposing fungi, suggesting a possible role for AA3_2s in lignin oxidation and degradation [ 27 ].…”

Methionine oxidation of Carbohydrate-Active enZymes during white-rot wood decay

“…H 2 O 2 is generated by glucose-methanol-choline oxidoreductases (AA3) and copper radical oxidases (AA5), that target carbohydrate or aliphatic/aromatic alcohols (11,12). In white-rot fungi, H 2 O 2 acts as a co-substrate to fuel different types of LPMOs and AA2 peroxidases (13)(14)(15). While the roles of CAZymes and H 2 O 2 during the degradation of lignocellulose is welldocumented, the impact of ROS on the oxidation of CAZymes remains unclear.…”