Evolution of Fungal Carbohydrate-Active Enzyme Portfolios and Adaptation to Plant Cell-Wall Polymers

Hayat Hage,Marie-Noëlle Rosso

doi:10.3390/jof7030185

Abstract

The postindustrial era is currently facing two ecological challenges. First, the rise in global temperature, mostly caused by the accumulation of carbon dioxide (CO2) in the atmosphere, and second, the inability of the environment to absorb the waste of human activities. Fungi are valuable levers for both a reduction in CO2 emissions, and the improvement of a circular economy with the optimized valorization of plant waste and biomass. Soil fungi may promote plant growth and thereby increase CO2 assimilation via photosynthesis or, conversely, they may prompt the decomposition of dead organic matter, and thereby contribute to CO2 emissions. The strategies that fungi use to cope with plant-cell-wall polymers and access the saccharides that they use as a carbon source largely rely on the secretion of carbohydrate-active enzymes (CAZymes). In the past few years, comparative genomics and phylogenomics coupled with the functional characterization of CAZymes significantly improved the understanding of their evolution in fungal genomes, providing a framework for the design of nature-inspired enzymatic catalysts. Here, we provide an overview of the diversity of CAZyme enzymatic systems employed by fungi that exhibit different substrate preferences, different ecologies, or belong to different taxonomical groups for lignocellulose degradation.

Highlights

The massive population growth that the world faces today is causing an increase in greenhouse gas emissions, of which carbon dioxide (CO2), methane (CH4), nitrous oxide (N2O), and fluorinated gases (F-gases) are the most significant
We review recent findings on the enzymatic systems used by fungi for lignocellulose degradation, with an emphasis on wood-decay fungi from the order of Polyporales, which remains a focus of research efforts in recent years
The adaptation of Agaricales to diverse ecological niches parallels a surprisingly high-protein sequence diversification in ligninolytic peroxidases, which evolved from an ancestral MnP isoform to MnP, versatile peroxidase (VP), and lignin peroxidase (LiP) isoforms, with diverse protein lengths and amino acids engaged at the catalytic site [38]

Summary

Introduction

The massive population growth that the world faces today is causing an increase in greenhouse gas emissions, of which carbon dioxide (CO2), methane (CH4), nitrous oxide (N2O), and fluorinated gases (F-gases) are the most significant. The pivotal role that white-rot fungi play in forest ecosystems stimulated research efforts to understand the enzymatic mechanisms involved in wood degradation. Another challenge for sustainability over time is the limited capability of the physical environment to absorb the waste of human activities. One solution lies in microorganisms that possess abilities to efficiently break down plant-cell-wall (PCW) polymers Of these microorganisms, fungi are the predominant source of enzymes currently used on an industrial scale for biomass transformation [14]. Fungi that use plant tissue as a carbon source acquired a large diversity of PCW-degrading or -modifying enzymes (PCWDE; Table 1). FAD-dependent (GMC) oxidoreductase vanillin alcohol oxidase copper radical oxidase benzoquinon reductase glycooligosaccharide oxidase pyrroloquinoline quinone-dependent oxidoreductase

Fungal Adaptations to Land Plants Paralleled by Evolution of Fungal CAZomes

Polyporales

Litter-Decay Fungi

CAZomes of Mycorrhizal Fungi

Findings

Conclusions