Abstract
Fungi contain a remarkable range of metabolic pathways, sometimes encoded by gene clusters, enabling them to digest most organic matter and synthesize an array of potent small molecules. Although metabolism is fundamental to the fungal lifestyle, we still know little about how major evolutionary processes, such as gene duplication (GD) and horizontal gene transfer (HGT), have interacted with clustered and non-clustered fungal metabolic pathways to give rise to this metabolic versatility. We examined the synteny and evolutionary history of 247,202 fungal genes encoding enzymes that catalyze 875 distinct metabolic reactions from 130 pathways in 208 diverse genomes. We found that gene clustering varied greatly with respect to metabolic category and lineage; for example, clustered genes in Saccharomycotina yeasts were overrepresented in nucleotide metabolism, whereas clustered genes in Pezizomycotina were more common in lipid and amino acid metabolism. The effects of both GD and HGT were more pronounced in clustered genes than in their non-clustered counterparts and were differentially distributed across fungal lineages; specifically, GD, which was an order of magnitude more abundant than HGT, was most frequently observed in Agaricomycetes, whereas HGT was much more prevalent in Pezizomycotina. The effect of HGT in some Pezizomycotina was particularly strong; for example, we identified 111 HGT events associated with the 15 Aspergillus genomes, which sharply contrasts with the 60 HGT events detected for the 48 genomes from the entire Saccharomycotina subphylum. Finally, the impact of GD within a metabolic category was typically consistent across all fungal lineages, whereas the impact of HGT was variable. These results indicate that GD is the dominant process underlying fungal metabolic diversity, whereas HGT is episodic and acts in a category- or lineage-specific manner. Both processes have a greater impact on clustered genes, suggesting that metabolic gene clusters represent hotspots for the generation of fungal metabolic diversity.
Highlights
As one of the primary decomposers of organic material in nature, fungal species catabolize a wide diversity of substrates [1], including cellulose and lignin, the two most abundant biopolymers on earth [2]
Examination of fungal metabolism for the presence of metabolic gene clusters revealed that 3.0% (7,409) of ECgenes belonged to 3,408 distinct gene clusters, with the average genome containing 16.7 metabolic gene clusters and 36.3 clustered ECgenes (Table S3)
Determining the relative role of gene duplication (GD) and horizontal gene transfer (HGT) with clustered and non-clustered metabolic pathways is important for understanding the evolution of the fungal metabolic repertoire
Summary
As one of the primary decomposers of organic material in nature, fungal species catabolize a wide diversity of substrates [1], including cellulose and lignin, the two most abundant biopolymers on earth [2]. Fungal metabolites have historically been divided into primary, that is metabolites essential for growth and reproduction, and secondary, which include ecologically important metabolites not essential to cellular life [7,8]. This distinction is arbitrary when applied to metabolic pathways rather than their products because the essentiality of a given pathway is speciesspecific [9] and because the pathways that generate primary and secondary metabolites are not mutually exclusive [10,11]. Fungal metabolic gene clusters participate in diverse activities including nitrogen [16,17], carbohydrate [18], amino acid [19], and vitamin [12] metabolism as well as in xenobiotic catabolism [11,20] and the biosynthesis of secondary metabolites [e.g., 21–28]
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