Who is your neighbor?
Gene clusters are groups of genes that remain in close neighborhood across large evolutionary distances, and despite pervasive genomic re-arrangements. In prokaryotes (organisms with anucleated cells like bacteria) such clusters may consist in operons, groups of genes that are co-transcribed in a single transcript and translated together to ensure their tight co-regulation. In eukaryotes (organisms with cells with a nucleus like plants, fungi, and animals), despite the abscence of true operons, there are examples of clusters of co-regulated genes mostly involved in secondary metabolism. However, very little is known about how gene clustering patterns vary among taxa or with respect to functional roles. Furthermore, mechanisms of the formation, maintenance and evolution of gene clusters remain unknown.
We set out to study this in fungi, the eukaryotic group that is best sampled in terms of fully-sequenced genomes. We surveyed 341 fungal genomes to discover gene clusters shared by different species, independently of their functions. We inferred 12,120 cluster families, which comprised roughly one third of the gene space and were enriched in genes associated with diverse cellular functions. Additionally, most clusters did not encode transcription factors, suggesting that they are regulated distally. We used phylogenomics to characterize the evolutionary history of these clusters. We found that most clusters originated once and were transmitted vertically, coupled to differential loss. However, convergent evolution, that is, independent appearance of the same cluster, was more prevalent than anticipated. Finally, horizontal gene transfer of entire clusters was somewhat restricted, with the exception of those associated with secondary metabolism. Altogether, our results provide insights on the evolution of gene clustering as well as a broad catalogue of evolutionarily conserved gene clusters whose function remains to be elucidated.