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Several genes encoding enzymes with the same activity are necessary for aerobic fungal degradation of cellulose in nature.

Busk PK, Lange M, Pilgaard B, Lange L - PLoS ONE (2014)

Bottom Line: Furthermore, a high number of AA9, endocellulase and β-glucosidase genes were identified, not in what are known to be the strongest, specialized lignocellulose degraders but in saprophytic fungi that can use a wide variety of substrates whereas only few of these genes were found in fungi that have a limited number of natural, lignocellulotic substrates.This correlation suggests that enzymes with different properties are necessary for degradation of cellulose in different complex substrates.Interestingly, clustering of the fungi based on their predicted enzymes indicated that Ascomycota and Basidiomycota use the same enzymatic activities to degrade plant cell walls.

View Article: PubMed Central - PubMed

Affiliation: Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, A.C. Meyers Vænge 15, 2450, Copenhagen SV, Denmark.

ABSTRACT
The cellulose-degrading fungal enzymes are glycoside hydrolases of the GH families and lytic polysaccharide monooxygenases. The entanglement of glycoside hydrolase families and functions makes it difficult to predict the enzymatic activity of glycoside hydrolases based on their sequence. In the present study we further developed the method Peptide Pattern Recognition to an automatic approach not only to find all genes encoding glycoside hydrolases and lytic polysaccharide monooxygenases in fungal genomes but also to predict the function of the genes. The functional annotation is an important feature as it provides a direct route to predict function from primary sequence. Furthermore, we used Peptide Pattern Recognition to compare the cellulose-degrading enzyme activities encoded by 39 fungal genomes. The results indicated that cellobiohydrolases and AA9 lytic polysaccharide monooxygenases are hallmarks of cellulose-degrading fungi except brown rot fungi. Furthermore, a high number of AA9, endocellulase and β-glucosidase genes were identified, not in what are known to be the strongest, specialized lignocellulose degraders but in saprophytic fungi that can use a wide variety of substrates whereas only few of these genes were found in fungi that have a limited number of natural, lignocellulotic substrates. This correlation suggests that enzymes with different properties are necessary for degradation of cellulose in different complex substrates. Interestingly, clustering of the fungi based on their predicted enzymes indicated that Ascomycota and Basidiomycota use the same enzymatic activities to degrade plant cell walls.

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Average number of genes encoding glycoside hydrolase and LPMO enzymes in the 39 fungi.The average number of genes predicted to encode cellulose-degrading activities (EC 3.2.1.4, 3.2.1.21, EC 3.2.1.91 and EC 3.2.1.176 and LPMOs), hemicellulose-degrading activities (EC 3.2.1.37, 3.2.1.151, 3.2.1.8, 3.2.1.55, 3.2.1.23, 3.2.1.59, 3.2.1.131, 3.2.1.177, 3.2.1.78, 3.2.1.67, 2.4.1.183, 3.2.1.25, 3.2.1.31, 3.2.1.15, 3.2.1.39, 3.2.1.58, 3.2.1.63, 3.2.1.22, 3.2.1.99, 3.2.1.75, 3.2.1.52, 3.2.1.6, 3.2.1.106, 3.2.1.51, 3.2.1.113, 2.4.1.18, 2.4.1.25, 3.2.1.28, 3.2.1.45, 3.2.1.18, 3.2.1.3, 3.2.1.26, 3.2.1.24, 2.4.1.20, 3.2.1.40 and 3.2.1.171) or other activities (EC 3.2.1.1, 3.2.1.20, 3.2.1.10, 3.2.1.165, 3.2.1.132, 3.2.1.14, 3.2.1.145, 3.2.1.89 and 3.2.1.164) in the cellulose-degraders and non-cellulose degraders. The division of enzyme activities (EC numbers) on cellulose-degradation, hemicellulose-degradation or other was described previously [2].
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pone-0114138-g006: Average number of genes encoding glycoside hydrolase and LPMO enzymes in the 39 fungi.The average number of genes predicted to encode cellulose-degrading activities (EC 3.2.1.4, 3.2.1.21, EC 3.2.1.91 and EC 3.2.1.176 and LPMOs), hemicellulose-degrading activities (EC 3.2.1.37, 3.2.1.151, 3.2.1.8, 3.2.1.55, 3.2.1.23, 3.2.1.59, 3.2.1.131, 3.2.1.177, 3.2.1.78, 3.2.1.67, 2.4.1.183, 3.2.1.25, 3.2.1.31, 3.2.1.15, 3.2.1.39, 3.2.1.58, 3.2.1.63, 3.2.1.22, 3.2.1.99, 3.2.1.75, 3.2.1.52, 3.2.1.6, 3.2.1.106, 3.2.1.51, 3.2.1.113, 2.4.1.18, 2.4.1.25, 3.2.1.28, 3.2.1.45, 3.2.1.18, 3.2.1.3, 3.2.1.26, 3.2.1.24, 2.4.1.20, 3.2.1.40 and 3.2.1.171) or other activities (EC 3.2.1.1, 3.2.1.20, 3.2.1.10, 3.2.1.165, 3.2.1.132, 3.2.1.14, 3.2.1.145, 3.2.1.89 and 3.2.1.164) in the cellulose-degraders and non-cellulose degraders. The division of enzyme activities (EC numbers) on cellulose-degradation, hemicellulose-degradation or other was described previously [2].

Mentions: Several of the gene families encoding hemicellulose-degrading enzymes such as xylan 1,4-beta-xylosidase, xyloglucan-specific endo-beta-1,4-glucanase, endo-1,4-beta-xylanase and alpha-N-arabinofuranosidase showed the same pattern of occurrence as the cellulases with one or more genes in almost all the cellulose-degraders, fewest in the brown rot fungi, and no genes in most of the non-degraders (Fig. 6, Table S6). In contrast genes encoding enzymes such as α-amylase or chitinase that attack other types of carbohydrate macrostructures followed a different pattern of occurrence.


Several genes encoding enzymes with the same activity are necessary for aerobic fungal degradation of cellulose in nature.

Busk PK, Lange M, Pilgaard B, Lange L - PLoS ONE (2014)

Average number of genes encoding glycoside hydrolase and LPMO enzymes in the 39 fungi.The average number of genes predicted to encode cellulose-degrading activities (EC 3.2.1.4, 3.2.1.21, EC 3.2.1.91 and EC 3.2.1.176 and LPMOs), hemicellulose-degrading activities (EC 3.2.1.37, 3.2.1.151, 3.2.1.8, 3.2.1.55, 3.2.1.23, 3.2.1.59, 3.2.1.131, 3.2.1.177, 3.2.1.78, 3.2.1.67, 2.4.1.183, 3.2.1.25, 3.2.1.31, 3.2.1.15, 3.2.1.39, 3.2.1.58, 3.2.1.63, 3.2.1.22, 3.2.1.99, 3.2.1.75, 3.2.1.52, 3.2.1.6, 3.2.1.106, 3.2.1.51, 3.2.1.113, 2.4.1.18, 2.4.1.25, 3.2.1.28, 3.2.1.45, 3.2.1.18, 3.2.1.3, 3.2.1.26, 3.2.1.24, 2.4.1.20, 3.2.1.40 and 3.2.1.171) or other activities (EC 3.2.1.1, 3.2.1.20, 3.2.1.10, 3.2.1.165, 3.2.1.132, 3.2.1.14, 3.2.1.145, 3.2.1.89 and 3.2.1.164) in the cellulose-degraders and non-cellulose degraders. The division of enzyme activities (EC numbers) on cellulose-degradation, hemicellulose-degradation or other was described previously [2].
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4252092&req=5

pone-0114138-g006: Average number of genes encoding glycoside hydrolase and LPMO enzymes in the 39 fungi.The average number of genes predicted to encode cellulose-degrading activities (EC 3.2.1.4, 3.2.1.21, EC 3.2.1.91 and EC 3.2.1.176 and LPMOs), hemicellulose-degrading activities (EC 3.2.1.37, 3.2.1.151, 3.2.1.8, 3.2.1.55, 3.2.1.23, 3.2.1.59, 3.2.1.131, 3.2.1.177, 3.2.1.78, 3.2.1.67, 2.4.1.183, 3.2.1.25, 3.2.1.31, 3.2.1.15, 3.2.1.39, 3.2.1.58, 3.2.1.63, 3.2.1.22, 3.2.1.99, 3.2.1.75, 3.2.1.52, 3.2.1.6, 3.2.1.106, 3.2.1.51, 3.2.1.113, 2.4.1.18, 2.4.1.25, 3.2.1.28, 3.2.1.45, 3.2.1.18, 3.2.1.3, 3.2.1.26, 3.2.1.24, 2.4.1.20, 3.2.1.40 and 3.2.1.171) or other activities (EC 3.2.1.1, 3.2.1.20, 3.2.1.10, 3.2.1.165, 3.2.1.132, 3.2.1.14, 3.2.1.145, 3.2.1.89 and 3.2.1.164) in the cellulose-degraders and non-cellulose degraders. The division of enzyme activities (EC numbers) on cellulose-degradation, hemicellulose-degradation or other was described previously [2].
Mentions: Several of the gene families encoding hemicellulose-degrading enzymes such as xylan 1,4-beta-xylosidase, xyloglucan-specific endo-beta-1,4-glucanase, endo-1,4-beta-xylanase and alpha-N-arabinofuranosidase showed the same pattern of occurrence as the cellulases with one or more genes in almost all the cellulose-degraders, fewest in the brown rot fungi, and no genes in most of the non-degraders (Fig. 6, Table S6). In contrast genes encoding enzymes such as α-amylase or chitinase that attack other types of carbohydrate macrostructures followed a different pattern of occurrence.

Bottom Line: Furthermore, a high number of AA9, endocellulase and β-glucosidase genes were identified, not in what are known to be the strongest, specialized lignocellulose degraders but in saprophytic fungi that can use a wide variety of substrates whereas only few of these genes were found in fungi that have a limited number of natural, lignocellulotic substrates.This correlation suggests that enzymes with different properties are necessary for degradation of cellulose in different complex substrates.Interestingly, clustering of the fungi based on their predicted enzymes indicated that Ascomycota and Basidiomycota use the same enzymatic activities to degrade plant cell walls.

View Article: PubMed Central - PubMed

Affiliation: Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, A.C. Meyers Vænge 15, 2450, Copenhagen SV, Denmark.

ABSTRACT
The cellulose-degrading fungal enzymes are glycoside hydrolases of the GH families and lytic polysaccharide monooxygenases. The entanglement of glycoside hydrolase families and functions makes it difficult to predict the enzymatic activity of glycoside hydrolases based on their sequence. In the present study we further developed the method Peptide Pattern Recognition to an automatic approach not only to find all genes encoding glycoside hydrolases and lytic polysaccharide monooxygenases in fungal genomes but also to predict the function of the genes. The functional annotation is an important feature as it provides a direct route to predict function from primary sequence. Furthermore, we used Peptide Pattern Recognition to compare the cellulose-degrading enzyme activities encoded by 39 fungal genomes. The results indicated that cellobiohydrolases and AA9 lytic polysaccharide monooxygenases are hallmarks of cellulose-degrading fungi except brown rot fungi. Furthermore, a high number of AA9, endocellulase and β-glucosidase genes were identified, not in what are known to be the strongest, specialized lignocellulose degraders but in saprophytic fungi that can use a wide variety of substrates whereas only few of these genes were found in fungi that have a limited number of natural, lignocellulotic substrates. This correlation suggests that enzymes with different properties are necessary for degradation of cellulose in different complex substrates. Interestingly, clustering of the fungi based on their predicted enzymes indicated that Ascomycota and Basidiomycota use the same enzymatic activities to degrade plant cell walls.

Show MeSH
Related in: MedlinePlus