The evolution of fungal metabolic pathways

PLoS Genet. 2014 Dec 4;10(12):e1004816. doi: 10.1371/journal.pgen.1004816. eCollection 2014 Dec.


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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ascomycota / genetics
  • Evolution, Molecular*
  • Gene Duplication
  • Gene Regulatory Networks
  • Gene Transfer, Horizontal
  • Genes, Fungal
  • Genome, Fungal*
  • Metabolic Networks and Pathways / genetics*
  • Multigene Family
  • Phylogeny

Grant support

This work was conducted in part using the resources of the Advanced Computing Center for Research and Education at Vanderbilt University, Nashville, TN. This work was partially supported by funds provided by the National Science Foundation (, grants IOS-1401682 to JHW, DBI-0805625 to JCS and DEB-0844968 to AR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.