Metabolic Specialization and Codon Preference of Lignocellulolytic Genes in the White Rot Basidiomycete Ceriporiopsis subvermispora.

Alex Gonzalez,Gino Corsini,Mario Tello,Daniela Seelenfreund,Sergio Lobos

doi:10.3390/genes11101227

Alex Gonzalez, Gino Corsini + Show 3 more

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https://doi.org/10.3390/genes11101227

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Abstract

Ceriporiopsis subvermispora is a white-rot fungus with a high specificity towards lignin mineralization when colonizing dead wood or lignocellulosic compounds. Its lignocellulose degrading system is formed by cellulose hydrolytic enzymes, manganese peroxidases, and laccases that catalyze the efficient depolymerization and mineralization of lignocellulose. To determine if this metabolic specialization has modified codon usage of the lignocellulolytic system, improving its adaptation to the fungal translational machine, we analyzed the adaptation to host codon usage (CAI), tRNA pool (tAI, and AAtAI), codon pair bias (CPB), and the number of effective codons (Nc). These indexes were correlated with gene expression of C. subvermispora, in the presence of glucose and Aspen wood. General gene expression was not correlated with the index values. However, in media containing Aspen wood, the induction of expression of lignocellulose-degrading genes, showed significantly (p < 0.001) higher values of CAI, AAtAI, CPB, tAI, and lower values of Nc than non-induced genes. Cellulose-binding proteins and manganese peroxidases presented the highest adaptation values. We also identified an expansion of genes encoding glycine and glutamic acid tRNAs. Our results suggest that the metabolic specialization to use wood as the sole carbon source has introduced a bias in the codon usage of genes involved in lignocellulose degradation. This bias reduces codon diversity and increases codon usage adaptation to the tRNA pool available in C. subvermispora. To our knowledge, this is the first study showing that codon usage is modified to improve the translation efficiency of a group of genes involved in a particular metabolic process.

Highlights

The main carbon source synthesized through photosynthesis which plays a central role in the carbon cycle of the planet is lignocellulose
Our results show that selective pressure imposed by the use of lignocellulose has modified codon usage of genes involved in the utilization of lignocellulose, favoring an increase in translational efficiency with respect to genes not involved in this process
Genome analysis of C. subvermispora by tRNAScan-SE identified a total of 192 tRNAs in 32 scaffolds (Figure 1)

Summary

Introduction

The main carbon source synthesized through photosynthesis which plays a central role in the carbon cycle of the planet is lignocellulose. A small group of filamentous fungi from the basidiomycete phylum is unique in its ability to efficiently degrade lignocellulose [1]. Together they are collectively known as white rot fungi, developing an enzymatic machinery that allows degradation of the three main components of lignocellulose: lignin, cellulose, and hemicellulose. Genes 2020, 11, 1227 hemicellulose, whose sugar moieties are used as carbon and energy sources. Degradation of these aromatic and carbohydrate polymers progresses by different mechanisms. While mineralization of lignin is carried out by free radicals generated enzymatically [2,3], the degradation of cellulose and hemicellulose into its constituent sugars occurs through the combination of direct enzymatic hydrolysis and partial hydrolysis by enzymatically generated free radicals [4]

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