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Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii

The experimental evolution of microorganisms exposed to extreme conditions can provide insight into cellular adaptation to stress. Typically, stress-sensitive species are exposed to stress over many generations and then examined for improvements in their stress tolerance. In contrast, when starting...

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Autores principales: Gostinčar, Cene, Stajich, Jason E., Kejžar, Anja, Sinha, Sunita, Nislow, Corey, Lenassi, Metka, Gunde-Cimerman, Nina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8468603/
https://www.ncbi.nlm.nih.gov/pubmed/34575761
http://dx.doi.org/10.3390/jof7090723
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author Gostinčar, Cene
Stajich, Jason E.
Kejžar, Anja
Sinha, Sunita
Nislow, Corey
Lenassi, Metka
Gunde-Cimerman, Nina
author_facet Gostinčar, Cene
Stajich, Jason E.
Kejžar, Anja
Sinha, Sunita
Nislow, Corey
Lenassi, Metka
Gunde-Cimerman, Nina
author_sort Gostinčar, Cene
collection PubMed
description The experimental evolution of microorganisms exposed to extreme conditions can provide insight into cellular adaptation to stress. Typically, stress-sensitive species are exposed to stress over many generations and then examined for improvements in their stress tolerance. In contrast, when starting with an already stress-tolerant progenitor there may be less room for further improvement, it may still be able to tweak its cellular machinery to increase extremotolerance, perhaps at the cost of poorer performance under non-extreme conditions. To investigate these possibilities, a strain of extremely halotolerant black yeast Hortaea werneckii was grown for over seven years through at least 800 generations in a medium containing 4.3 M NaCl. Although this salinity is well above the optimum (0.8–1.7 M) for the species, the growth rate of the evolved H. werneckii did not change in the absence of salt or at high concentrations of NaCl, KCl, sorbitol, or glycerol. Other phenotypic traits did change during the course of the experimental evolution, including fewer multicellular chains in the evolved strains, significantly narrower cells, increased resistance to caspofungin, and altered melanisation. Whole-genome sequencing revealed the occurrence of multiple aneuploidies during the experimental evolution of the otherwise diploid H. werneckii. A significant overrepresentation of several gene groups was observed in aneuploid regions. Taken together, these changes suggest that long-term growth at extreme salinity led to alterations in cell wall and morphology, signalling pathways, and the pentose phosphate cycle. Although there is currently limited evidence for the adaptive value of these changes, they offer promising starting points for future studies of fungal halotolerance.
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spelling pubmed-84686032021-09-27 Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii Gostinčar, Cene Stajich, Jason E. Kejžar, Anja Sinha, Sunita Nislow, Corey Lenassi, Metka Gunde-Cimerman, Nina J Fungi (Basel) Article The experimental evolution of microorganisms exposed to extreme conditions can provide insight into cellular adaptation to stress. Typically, stress-sensitive species are exposed to stress over many generations and then examined for improvements in their stress tolerance. In contrast, when starting with an already stress-tolerant progenitor there may be less room for further improvement, it may still be able to tweak its cellular machinery to increase extremotolerance, perhaps at the cost of poorer performance under non-extreme conditions. To investigate these possibilities, a strain of extremely halotolerant black yeast Hortaea werneckii was grown for over seven years through at least 800 generations in a medium containing 4.3 M NaCl. Although this salinity is well above the optimum (0.8–1.7 M) for the species, the growth rate of the evolved H. werneckii did not change in the absence of salt or at high concentrations of NaCl, KCl, sorbitol, or glycerol. Other phenotypic traits did change during the course of the experimental evolution, including fewer multicellular chains in the evolved strains, significantly narrower cells, increased resistance to caspofungin, and altered melanisation. Whole-genome sequencing revealed the occurrence of multiple aneuploidies during the experimental evolution of the otherwise diploid H. werneckii. A significant overrepresentation of several gene groups was observed in aneuploid regions. Taken together, these changes suggest that long-term growth at extreme salinity led to alterations in cell wall and morphology, signalling pathways, and the pentose phosphate cycle. Although there is currently limited evidence for the adaptive value of these changes, they offer promising starting points for future studies of fungal halotolerance. MDPI 2021-09-04 /pmc/articles/PMC8468603/ /pubmed/34575761 http://dx.doi.org/10.3390/jof7090723 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Gostinčar, Cene
Stajich, Jason E.
Kejžar, Anja
Sinha, Sunita
Nislow, Corey
Lenassi, Metka
Gunde-Cimerman, Nina
Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title_full Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title_fullStr Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title_full_unstemmed Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title_short Seven Years at High Salinity—Experimental Evolution of the Extremely Halotolerant Black Yeast Hortaea werneckii
title_sort seven years at high salinity—experimental evolution of the extremely halotolerant black yeast hortaea werneckii
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8468603/
https://www.ncbi.nlm.nih.gov/pubmed/34575761
http://dx.doi.org/10.3390/jof7090723
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