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A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event

BACKGROUND: Horizontal gene transfer (HGT) is an evolutionary mechanism of adaptive importance, which has been deeply studied in wine S. cerevisiae strains, where those acquired genes conferred improved traits related to both transport and metabolism of the nutrients present in the grape must. Howev...

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Autores principales: Tapia, Sebastián M., Macías, Laura G., Pérez-Torrado, Roberto, Daroqui, Noemi, Manzanares, Paloma, Querol, Amparo, Barrio, Eladio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10169451/
https://www.ncbi.nlm.nih.gov/pubmed/37158891
http://dx.doi.org/10.1186/s12915-023-01566-6
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author Tapia, Sebastián M.
Macías, Laura G.
Pérez-Torrado, Roberto
Daroqui, Noemi
Manzanares, Paloma
Querol, Amparo
Barrio, Eladio
author_facet Tapia, Sebastián M.
Macías, Laura G.
Pérez-Torrado, Roberto
Daroqui, Noemi
Manzanares, Paloma
Querol, Amparo
Barrio, Eladio
author_sort Tapia, Sebastián M.
collection PubMed
description BACKGROUND: Horizontal gene transfer (HGT) is an evolutionary mechanism of adaptive importance, which has been deeply studied in wine S. cerevisiae strains, where those acquired genes conferred improved traits related to both transport and metabolism of the nutrients present in the grape must. However, little is known about HGT events that occurred in wild Saccharomyces yeasts and how they determine their phenotypes. RESULTS: Through a comparative genomic approach among Saccharomyces species, we detected a subtelomeric segment present in the S. uvarum, S. kudriavzevii, and S. eubayanus species, belonging to the first species to diverge in the Saccharomyces genus, but absent in the other Saccharomyces species. The segment contains three genes, two of which were characterized, named DGD1 and DGD2. DGD1 encodes dialkylglicine decarboxylase, whose specific substrate is the non-proteinogenic amino acid 2-aminoisobutyric acid (AIB), a rare amino acid present in some antimicrobial peptides of fungal origin. DGD2 encodes putative zinc finger transcription factor, which is essential to induce the AIB-dependent expression of DGD1. Phylogenetic analysis showed that DGD1 and DGD2 are closely related to two adjacent genes present in Zygosaccharomyces. CONCLUSIONS: The presented results show evidence of an early HGT event conferring new traits to the ancestor of the Saccharomyces genus that could be lost in the evolutionary more recent Saccharomyces species, perhaps due to loss of function during the colonization of new habitats. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01566-6.
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spelling pubmed-101694512023-05-11 A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event Tapia, Sebastián M. Macías, Laura G. Pérez-Torrado, Roberto Daroqui, Noemi Manzanares, Paloma Querol, Amparo Barrio, Eladio BMC Biol Research Article BACKGROUND: Horizontal gene transfer (HGT) is an evolutionary mechanism of adaptive importance, which has been deeply studied in wine S. cerevisiae strains, where those acquired genes conferred improved traits related to both transport and metabolism of the nutrients present in the grape must. However, little is known about HGT events that occurred in wild Saccharomyces yeasts and how they determine their phenotypes. RESULTS: Through a comparative genomic approach among Saccharomyces species, we detected a subtelomeric segment present in the S. uvarum, S. kudriavzevii, and S. eubayanus species, belonging to the first species to diverge in the Saccharomyces genus, but absent in the other Saccharomyces species. The segment contains three genes, two of which were characterized, named DGD1 and DGD2. DGD1 encodes dialkylglicine decarboxylase, whose specific substrate is the non-proteinogenic amino acid 2-aminoisobutyric acid (AIB), a rare amino acid present in some antimicrobial peptides of fungal origin. DGD2 encodes putative zinc finger transcription factor, which is essential to induce the AIB-dependent expression of DGD1. Phylogenetic analysis showed that DGD1 and DGD2 are closely related to two adjacent genes present in Zygosaccharomyces. CONCLUSIONS: The presented results show evidence of an early HGT event conferring new traits to the ancestor of the Saccharomyces genus that could be lost in the evolutionary more recent Saccharomyces species, perhaps due to loss of function during the colonization of new habitats. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01566-6. BioMed Central 2023-05-08 /pmc/articles/PMC10169451/ /pubmed/37158891 http://dx.doi.org/10.1186/s12915-023-01566-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Tapia, Sebastián M.
Macías, Laura G.
Pérez-Torrado, Roberto
Daroqui, Noemi
Manzanares, Paloma
Querol, Amparo
Barrio, Eladio
A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title_full A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title_fullStr A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title_full_unstemmed A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title_short A novel aminotransferase gene and its regulator acquired in Saccharomyces by a horizontal gene transfer event
title_sort novel aminotransferase gene and its regulator acquired in saccharomyces by a horizontal gene transfer event
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10169451/
https://www.ncbi.nlm.nih.gov/pubmed/37158891
http://dx.doi.org/10.1186/s12915-023-01566-6
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