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Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization

Marco Mariotti, Didac Santesmasses, Salvador Capella-Gutierrez, Andrea Mateo, Carme Arnan, Rory Johnson, Salvatore D’Aniello, Sun Hee Yim, Vadim N Gladyshev, Florenci Serras, Montserrat Corominas, Toni Gabaldón, Roderic Guigé
doi: https://doi.org/10.1101/014928
Marco Mariotti
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
3Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), 08003 Barcelona, Catalonia, Spain
4Division of Genetics, Department of Medicine, Brigham & Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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  • For correspondence: roderic.guigo@crg.cat marco.mariotti@crg.cat
Didac Santesmasses
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
3Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), 08003 Barcelona, Catalonia, Spain
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Salvador Capella-Gutierrez
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
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Andrea Mateo
5Departament de Genètica, Facultat de Biologia and Institut de Biomedicina (IBUB) de la Universitat de Barcelona (UB), 08028 Barcelona, Catalonia, Spain
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Carme Arnan
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
3Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), 08003 Barcelona, Catalonia, Spain
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Rory Johnson
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
3Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), 08003 Barcelona, Catalonia, Spain
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Salvatore D’Aniello
6Cellular and Developmental Biology, Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy
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Sun Hee Yim
4Division of Genetics, Department of Medicine, Brigham & Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Vadim N Gladyshev
4Division of Genetics, Department of Medicine, Brigham & Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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Florenci Serras
5Departament de Genètica, Facultat de Biologia and Institut de Biomedicina (IBUB) de la Universitat de Barcelona (UB), 08028 Barcelona, Catalonia, Spain
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Montserrat Corominas
5Departament de Genètica, Facultat de Biologia and Institut de Biomedicina (IBUB) de la Universitat de Barcelona (UB), 08028 Barcelona, Catalonia, Spain
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Toni Gabaldón
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
7Institució Catalana de Recerca i Estudis Avançats (ICREA), Pg. Lluís Companys 23, 08010 Barcelona, Catalonia, Spain
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Roderic Guigé
1Bioinformatics and Genomics Programme, Centre for Genomic Regulation (CRG), Dr. Aiguader 88, 08003 Barcelona, Catalonia, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Catalonia, Spain
3Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), 08003 Barcelona, Catalonia, Spain
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  • For correspondence: roderic.guigo@crg.cat marco.mariotti@crg.cat
  • Abstract
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Abstract

SPS catalyzes the synthesis of selenophosphate, the selenium donor for the synthesis of the amino acid selenocysteine (Sec), incorporated in selenoproteins in response to the UGA codon. SPS is unique among proteins of the selenoprotein biosynthesis machinery in that it is, in many species, a selenoprotein itself, although, as in all selenoproteins, Sec is often replaced by cysteine (Cys). In metazoan genomes we found, however, SPS genes with lineage specific substitutions other than Sec or Cys. Our results show that these non-Sec, non-Cys SPS genes originated through a number of independent gene duplications of diverse molecular origin from an ancestral selenoprotein SPS gene. Although of independent origin, complementation assays in fly mutants show that these genes share a common function, which most likely emerged in the ancestral metazoan gene. This function appears to be unrelated to selenophosphate synthesis, since all genomes encoding selenoproteins contain Sec or Cys SPS genes (SPS2), but those containing only non-Sec, non-Cys SPS genes (SPS1) do not encode selenoproteins. Thus, in SPS genes, through parallel duplications and subsequent convergent subfunctionalization, two functions initially carried by a single gene are recurrently segregated at two different loci. RNA structures enhancing the readthrough of the Sec-UGA codon in SPS genes, which may be traced back to prokaryotes, played a key role in this process. The SPS evolutionary history in metazoans constitute a remarkable example of the emergence and evolution of gene function. We have been able to trace this history with unusual detail thanks to the singular feature of SPS genes, wherein the amino acid at a single site determines protein function, and, ultimately, the evolutionary fate of an entire class of genes.

  • Abbreviations used

    Sec
    selenocysteine
    Se
    selenium
    SeU
    selenouridine
    SeP
    selenophosphate
    SPS
    selenophosphate synthetase
    SelD
    selenophosphate synthetase (prokaryotes)
    SelA
    selenocysteine synthase (prokaryotes)
    ybbB
    selenouridine synthase (prokaryotes)
    Cys
    cysteine
    Arg
    arginine
    Thr
    threonine
    Gly
    glycine
    Leu
    leucine
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
    Marco Mariotti, Didac Santesmasses, Salvador Capella-Gutierrez, Andrea Mateo, Carme Arnan, Rory Johnson, Salvatore D’Aniello, Sun Hee Yim, Vadim N Gladyshev, Florenci Serras, Montserrat Corominas, Toni Gabaldón, Roderic Guigé
    bioRxiv 014928; doi: https://doi.org/10.1101/014928
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    Evolution of selenophosphate synthetases: emergence and relocation of function through independent duplications and recurrent subfunctionalization
    Marco Mariotti, Didac Santesmasses, Salvador Capella-Gutierrez, Andrea Mateo, Carme Arnan, Rory Johnson, Salvatore D’Aniello, Sun Hee Yim, Vadim N Gladyshev, Florenci Serras, Montserrat Corominas, Toni Gabaldón, Roderic Guigé
    bioRxiv 014928; doi: https://doi.org/10.1101/014928

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