Comparative Analysis of Peniophora lycii and Trametes hirsuta Exoproteomes Demonstrates “Shades of Gray” in the Concept of White-Rotting Fungi

Abstract

White-rot basidiomycete fungi are a unique group of organisms that evolved an unprecedented arsenal of extracellular enzymes for an efficient degradation of all components of wood such as cellulose, hemicelluloses and lignin. The exoproteomes of white-rot fungi represent a natural enzymatic toolbox for white biotechnology. Currently, only exoproteomes of a narrow taxonomic group of white-rot fungi—fungi belonging to the Polyporales order—are extensively studied. In this article, two white-rot fungi, Peniophora lycii LE-BIN 2142 from the Russulales order and Trametes hirsuta LE-BIN 072 from the Polyporales order, were compared and contrasted in terms of their enzymatic machinery used for degradation of different types of wood substrates—alder, birch and pine sawdust. Our findings suggested that the studied fungi use extremely different enzymatic systems for the degradation of carbohydrates and lignin. While T. hirsuta LE-BIN 072 behaved as a typical white-rot fungus, P. lycii LE-BIN 2142 demonstrated substantial peculiarities. Instead of using cellulolytic and hemicellulolytic hydrolytic enzymes, P. lycii LE-BIN 2142 primarily relies on oxidative polysaccharide-degrading enzymes such as LPMO and GMC oxidoreductase. Moreover, exoproteomes of P. lycii LE-BIN 2142 completely lacked ligninolytic peroxidases, a well-known marker of white-rot fungi, but instead contained several laccase isozymes and previously uncharacterized FAD-binding domain-containing proteins.

Exoproteomic Study and Transcriptional Responses of Laccase and Ligninolytic Peroxidase Genes of White-Rot Fungus Trametes hirsuta LE-BIN 072 Grown in the Presence of Monolignol-Related Phenolic Compounds

“…The obtained data confirm the hypothesis put forward earlier that lacA of T. hirsuta 072 is a gene that is expressed by default (i.e., "default on") [50]. As in the current study, in the studies where T. hirsuta 072 was cultivated on the media containing CuSO 4 , kraft lignin, synthetic dye (i.e., bromocresol green), lignocellulose and sawdust of various wood (i.e., alder, birch, or pine), LacA isozyme was always present in the fungal exoproteome (Supplementary Table S1) [38,49,51,52]. In addition, previous studies suggest that lacA may be regulated by both repressive and inductive mechanisms.…”

“…The first group of peroxidases contained isozymes that were present in all exoproteomes-VP2, MnP5, and MnP7. Interestingly, these three peroxidase isozymes were previously observed in almost all exoproteomes of T. hirsuta 072 ever published, including those obtained on kraft lignin, lignocellulose, bromocresol green, and sawdust of various wood (Supplementary Table S1) [38,49,51,52]. The only notable exception was the absence of MnP7 in exoproteomes obtained on the wood-containing media [52].…”

“…Interestingly, these three peroxidase isozymes were previously observed in almost all exoproteomes of T. hirsuta 072 ever published, including those obtained on kraft lignin, lignocellulose, bromocresol green, and sawdust of various wood (Supplementary Table S1) [38,49,51,52]. The only notable exception was the absence of MnP7 in exoproteomes obtained on the wood-containing media [52]. Possibly, expression of this isozyme was inhibited by the presence of cellulose, hemicellulose, or wood extractives.…”

Functional Characterization of Laccase Isozyme (PoLcc1) from the Edible Mushroom Pleurotus ostreatus Involved in Lignin Degradation in Cotton Straw

“…Studies have shown that the substrates cellulose: lignin ratios were found to be positively correlated to mycelial growth rates and to mushroom yield of P. ostreatus [ 30 , 31 ], and cotton straw is a substrate with high lignin content. In reports on cotton straw culture of edible mushrooms, it was found that higher yields could be obtained by applying to cotton straw culture of edible mushrooms relative to other crop substrates [ 32 , 33 , 34 , 35 ], in which lignin degrading enzymes played a crucial role [ 36 , 37 , 38 ]. In this study, we first screened the optimum culture conditions for laccase enzyme activity of P. ostreatus Suping 1.…”

First Description of Non-Enzymatic Radical-Generating Mechanisms Adopted by Fomitiporia mediterranea: An Unexplored Pathway of the White Rot Agent of the Esca Complex of Diseases

“…Fomitiporia mediterranea has historically been classified as a WRF [15]. In recent years, research has demonstrated how the binary classification of biomolecular decay mechanisms into either white rot or brown rot fungi is a "reductive monochromatic paradox" that does not represent all the nuances and peculiarities of Basidiomycota decay pathways [46][47][48]. In particular, as a WRF, Fmed presents a unique decay pattern fingerprint that results from a secretome that is unique in several different ways: i.…”