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Evolutionary and functional patterns of shared gene neighbourhood in fungi

Abstract

Gene clusters comprise genomically co-localized and potentially co-regulated genes that tend to be conserved across species. In eukaryotes, multiple examples of metabolic gene clusters are known, particularly among fungi and plants. However, 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 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.

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Fig. 1: Sunburst chart showing the percentage of clustered protein-coding genes per species.
Fig. 2: Example of gene cluster families classified as vertically evolving.
Fig. 3: Example of a gene cluster family classified as HGT.
Fig. 4: Example of a gene cluster family that has undergone convergent evolution.
Fig. 5

Data availability

All proteomes were downloaded from NCBI (April 2017). The full list of BioProjects can be found in Supplementary Table 1. All other data are available from the corresponding author upon request.

Code availability

EvolClust can be downloaded from our github repository: (https://github.com/Gabaldonlab/EvolClust/) and Evolclassifier can be found in the folder ‘additional scripts’ in the repository.

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Acknowledgements

The T.G. group acknowledges support from the Spanish Ministry of Economy, Industry and Competitiveness (MEIC) for the EMBL partnership, and grants ‘Centro de Excelencia Severo Ochoa 2013-2017’ SEV-2012-0208 and BFU2015-67107 cofounded by European Regional Development Fund (ERDF); from the CERCA Programme/Generalitat de Catalunya; from the Catalan Research Agency (AGAUR) SGR857, and a grant from the European Union’s Horizon 2020 research and innovation programme under grant agreement ERC-2016-724173 the Marie Sklodowska-Curie grant agreement H2020-MSCA-ITN-2014-642095.

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T.G. and M.M.-H. designed the study, M.M.-H. gathered the data and performed the cluster prediction and phylogenomics analysis. T.G. and M.M.-H. analysed the results and wrote the manuscript. T.G. supervised the study.

Corresponding author

Correspondence to Toni Gabaldón.

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Supplementary discussion and Supplementary Figs. 1–4.

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Supplementary Tables

Supplementary tables 1–19

Supplementary Table 2

List of predicted clusters

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Marcet-Houben, M., Gabaldón, T. Evolutionary and functional patterns of shared gene neighbourhood in fungi. Nat Microbiol 4, 2383–2392 (2019). https://doi.org/10.1038/s41564-019-0552-0

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