Xenomic networks variability and adaptation traits in wood decaying fungi

Abstract

Fungal degradation of wood is mainly restricted to basidiomycetes, these organisms having developed complex oxidative and hydrolytic enzymatic systems. Besides these systems, wood-decaying fungi possess intracellular networks allowing them to deal with the myriad of potential toxic compounds resulting at least in part from wood degradation but also more generally from recalcitrant organic matter degradation. The members of the detoxification pathways constitute the xenome. Generally, they belong to multigenic families such as the cytochrome P450 monooxygenases and the glutathione transferases. Taking advantage of the recent release of numerous genomes of basidiomycetes, we show here that these multigenic families are extended and functionally related in wood-decaying fungi. Furthermore, we postulate that these rapidly evolving multigenic families could reflect the adaptation of these fungi to the diversity of their substrate and provide keys to understand their ecology. This is of particular importance for white biotechnology, this xenome being a putative target for improving degradation properties of these fungi in biomass valorization purposes.

Figure 1

The fungal detoxification system defined as ‘xenome’.

Figure 2

Phylogenetic tree of glutathione transferases from Basidiomycetes. Various subclasses could be distinguished: Ure2p, GSTFuA, Omega (GSTO), Glutathionyl Hydroquinone Reductase (GHR), Phi, GTT1 and GTT2. The sequences were retrieved from genomes available on the Joint Genome Institute (http://www.jgi.doe.gov/). Sequence alignments were done by clustalw and the tree was constructed with the neighbour-joining method in MEGA 5.0 software (Tamura et al., 2011). The robustness of the branches was assessed by the bootstrap method with 500 replications. The scale marker represents 0.2 substitutions per residue.

Figure 3

Organization of the GSTome in selected fungi. GST isoform numbers for each subclass are reported. The repartition has been done based on the sequences retrieved from the JGI coupled to phylogenetic analyses.

Figure 4

GSTome expansion in Agaricomycotina. A. Relative GSTome size of fungal species belonging to various phyla. The ratio between number of GST and number of gene models is reported. B. Relationship between GST and CytP450 copy numbers in the JGI available fungal genomes. Wood degraders exhibit the highest numbers of GST and CytP450 isoforms. Species names and data are given in supplemental Table S2.

Figure 5

Heat maps for selected P. carnosa transcripts coding for CytP450 (A) and GSTs (B), during growth on YMPG (Y) or medium containing wood from fir (F), pine (P), spruce (S) or maple (M), as determined by mRNA-Seq. The colour scale represents the reads per kilobase of gene model per million mapped reads. The figure has been adapted from MacDonald and colleagues (2011).