Abstract
Selenoproteins are a diverse group of proteins containing selenocysteine (Sec)—the twenty-first amino acid—incorporated during translation via a unique recoding mechanism1,2. Selenoproteins fulfil essential roles in many organisms1, yet are not ubiquitous across the tree of life3,4,5,6,7. In particular, fungi were deemed devoid of selenoproteins4,5,8. However, we show here that Sec is utilized by nine species belonging to diverse early-branching fungal phyla, as evidenced by the genomic presence of both Sec machinery and selenoproteins. Most fungal selenoproteins lack consensus Sec recoding signals (SECIS elements9) but exhibit other RNA structures, suggesting altered mechanisms of Sec insertion in fungi. Phylogenetic analyses support a scenario of vertical inheritance of the Sec trait within eukaryotes and fungi. Sec was then lost in numerous independent events in various fungal lineages. Notably, Sec was lost at the base of Dikarya, resulting in the absence of selenoproteins in Saccharomyces cerevisiae and other well-studied fungi. Our results indicate that, despite scattered occurrence, selenoproteins are found in all kingdoms of life.
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Code availability
The latest version of the selenoprotein gene finder software Selenoprofiles is available at https://github.com/marco-mariotti/selenoprofiles. The script ncbi_assembly, used to download NCBI assemblies in batch, is available at https://github.com/marco-mariotti/ncbi_db.
Data availability
A list of the fungal species and corresponding genomes (NCBI assembly accession IDs) used in this study is provided in Supplementary Table 1. Supplementary Data 1 contains the sequences of all of the genes and RNA elements mentioned in this work, as well as their genomic coordinates to derive these sequences from genomes. For each species, coordinates are mapped to GenBank nucleotide entries (contigs or scaffolds) found within their corresponding genome. Our re-annotated open reading frames are in the process of being assigned GenBank IDs.
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Acknowledgements
This work was supported by National Institutes of Health grants DK117149, AG021518 and CA080946. Funding for the open access charge was provided by the National Institutes of Health.
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G.S. first noted Sec machinery in a fungal genome and initiated this study. M.M. designed and performed the data analyses and wrote the manuscript. G.S., T.G. and V.N.G. participated in critical discussion and revised the manuscript.
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Supplementary information
Supplementary Information
Supplementary Figures 1–26 and Supplementary Notes.
Supplementary Table 1
Species names, assembly identifiers and taxonomic annotation of all fungal genomes analysed in this study.
Supplementary Table 2
Results of phylogenetic profiling to detect proteins related to Sec.
Supplementary Data 1 and 2
Sequences and genomic coordinates of Sec machinery, selenoproteins and RNA structures described in this work, and reconstructed phylogenetic trees of Sec machinery and selenoproteins (the same as in Fig. 3 and in Supplementary Figures 2–10) with branch support values.
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Mariotti, M., Salinas, G., Gabaldón, T. et al. Utilization of selenocysteine in early-branching fungal phyla. Nat Microbiol 4, 759–765 (2019). https://doi.org/10.1038/s41564-018-0354-9
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DOI: https://doi.org/10.1038/s41564-018-0354-9
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