Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation

The halotolerant yeast <i>Debaryomyces hansenii</i> belongs to the CTG-Ser1 clade of fungal species that use the CUG codon to translate as leucine or serine. The ambiguous decoding of the CUG codon is relevant for expanding protein diversity, but little is known about the role of leucine...

Full description

Bibliographic Details
Main Authors: Daniel Ochoa-Gutiérrez, Anya M. Reyes-Torres, Ileana de la Fuente-Colmenares, Viviana Escobar-Sánchez, James González, Rosario Ortiz-Hernández, Nayeli Torres-Ramírez, Claudia Segal-Kischinevzky
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/8/9/970
_version_ 1827659834249445376
author Daniel Ochoa-Gutiérrez
Anya M. Reyes-Torres
Ileana de la Fuente-Colmenares
Viviana Escobar-Sánchez
James González
Rosario Ortiz-Hernández
Nayeli Torres-Ramírez
Claudia Segal-Kischinevzky
author_facet Daniel Ochoa-Gutiérrez
Anya M. Reyes-Torres
Ileana de la Fuente-Colmenares
Viviana Escobar-Sánchez
James González
Rosario Ortiz-Hernández
Nayeli Torres-Ramírez
Claudia Segal-Kischinevzky
author_sort Daniel Ochoa-Gutiérrez
collection DOAJ
description The halotolerant yeast <i>Debaryomyces hansenii</i> belongs to the CTG-Ser1 clade of fungal species that use the CUG codon to translate as leucine or serine. The ambiguous decoding of the CUG codon is relevant for expanding protein diversity, but little is known about the role of leucine–serine ambiguity in cellular adaptations to extreme environments. Here, we examine sequences and structures of tRNA<sub>CAG</sub> from the CTG-Ser1 clade yeasts, finding that <i>D. hansenii</i> conserves the elements to translate ambiguously. Then, we show that <i>D. hansenii</i> has tolerance to conditions of salinity, acidity, alkalinity, and oxidative stress associated with phenotypic and ultrastructural changes. In these conditions, we found differential expression in both the logarithmic and stationary growth phases of tRNA<sup>Ser</sup>, tRNA<sup>Leu</sup>, tRNA<sub>CAG</sub>, LeuRS, and SerRS genes that could be involved in the adaptive process of this yeast. Finally, we compare the proteomic isoelectric points and hydropathy profiles, detecting that the most important variations among the physicochemical characteristics of <i>D. hansenii</i> proteins are in their hydrophobic and hydrophilic interactions with the medium. We propose that the ambiguous translation, i.e., leucylation or serynation, on translation of the CUG-encoded residues, could be linked to adaptation processes in extreme environments.
first_indexed 2024-03-09T23:29:50Z
format Article
id doaj.art-0153b23f8e49462eacbe6400167a7e87
institution Directory Open Access Journal
issn 2309-608X
language English
last_indexed 2024-03-09T23:29:50Z
publishDate 2022-09-01
publisher MDPI AG
record_format Article
series Journal of Fungi
spelling doaj.art-0153b23f8e49462eacbe6400167a7e872023-11-23T17:10:06ZengMDPI AGJournal of Fungi2309-608X2022-09-018997010.3390/jof8090970Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous TranslationDaniel Ochoa-Gutiérrez0Anya M. Reyes-Torres1Ileana de la Fuente-Colmenares2Viviana Escobar-Sánchez3James González4Rosario Ortiz-Hernández5Nayeli Torres-Ramírez6Claudia Segal-Kischinevzky7Laboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Microscopía Electrónica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Microscopía Electrónica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoLaboratorio de Biología Molecular y Genómica, Departamento de Biología Celular, Facultad de Ciencias, Universidad Nacional Autónoma de México, Avenida Universidad # 3000, Cd. Universitaria, Coyoacán, Mexico City 04510, MexicoThe halotolerant yeast <i>Debaryomyces hansenii</i> belongs to the CTG-Ser1 clade of fungal species that use the CUG codon to translate as leucine or serine. The ambiguous decoding of the CUG codon is relevant for expanding protein diversity, but little is known about the role of leucine–serine ambiguity in cellular adaptations to extreme environments. Here, we examine sequences and structures of tRNA<sub>CAG</sub> from the CTG-Ser1 clade yeasts, finding that <i>D. hansenii</i> conserves the elements to translate ambiguously. Then, we show that <i>D. hansenii</i> has tolerance to conditions of salinity, acidity, alkalinity, and oxidative stress associated with phenotypic and ultrastructural changes. In these conditions, we found differential expression in both the logarithmic and stationary growth phases of tRNA<sup>Ser</sup>, tRNA<sup>Leu</sup>, tRNA<sub>CAG</sub>, LeuRS, and SerRS genes that could be involved in the adaptive process of this yeast. Finally, we compare the proteomic isoelectric points and hydropathy profiles, detecting that the most important variations among the physicochemical characteristics of <i>D. hansenii</i> proteins are in their hydrophobic and hydrophilic interactions with the medium. We propose that the ambiguous translation, i.e., leucylation or serynation, on translation of the CUG-encoded residues, could be linked to adaptation processes in extreme environments.https://www.mdpi.com/2309-608X/8/9/970CTG-Ser1 cladeambiguous translationCUG codonmistranslationserynationleucylation
spellingShingle Daniel Ochoa-Gutiérrez
Anya M. Reyes-Torres
Ileana de la Fuente-Colmenares
Viviana Escobar-Sánchez
James González
Rosario Ortiz-Hernández
Nayeli Torres-Ramírez
Claudia Segal-Kischinevzky
Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
Journal of Fungi
CTG-Ser1 clade
ambiguous translation
CUG codon
mistranslation
serynation
leucylation
title Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
title_full Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
title_fullStr Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
title_full_unstemmed Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
title_short Alternative CUG Codon Usage in the Halotolerant Yeast <i>Debaryomyces hansenii</i>: Gene Expression Profiles Provide New Insights into Ambiguous Translation
title_sort alternative cug codon usage in the halotolerant yeast i debaryomyces hansenii i gene expression profiles provide new insights into ambiguous translation
topic CTG-Ser1 clade
ambiguous translation
CUG codon
mistranslation
serynation
leucylation
url https://www.mdpi.com/2309-608X/8/9/970
work_keys_str_mv AT danielochoagutierrez alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT anyamreyestorres alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT ileanadelafuentecolmenares alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT vivianaescobarsanchez alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT jamesgonzalez alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT rosarioortizhernandez alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT nayelitorresramirez alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation
AT claudiasegalkischinevzky alternativecugcodonusageinthehalotolerantyeastidebaryomyceshanseniiigeneexpressionprofilesprovidenewinsightsintoambiguoustranslation