Bacterial Evolution in High-Osmolarity Environments

ABSTRACT Bacteria must maintain a cytosolic osmolarity higher than that of their environment in order to take up water. High-osmolarity environments therefore present formidable stress to bacteria. To explore the evolutionary mechanisms by which bacteria adapt to high-osmolarity environments, we sel...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Spencer Cesar, Maya Anjur-Dietrich, Brian Yu, Ethan Li, Enrique Rojas, Norma Neff, Tim F. Cooper, Kerwyn Casey Huang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	stress response osmotic adaptation cell morphology cell shape proline sorbitol Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/774669d558a74ddf819033fab52029cf
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:774669d558a74ddf819033fab52029cf
record_format	dspace
spelling	oai:doaj.org-article:774669d558a74ddf819033fab52029cf2021-11-15T15:56:43ZBacterial Evolution in High-Osmolarity Environments10.1128/mBio.01191-202150-7511https://doaj.org/article/774669d558a74ddf819033fab52029cf2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01191-20https://doaj.org/toc/2150-7511ABSTRACT Bacteria must maintain a cytosolic osmolarity higher than that of their environment in order to take up water. High-osmolarity environments therefore present formidable stress to bacteria. To explore the evolutionary mechanisms by which bacteria adapt to high-osmolarity environments, we selected Escherichia coli in media with a variety of osmolytes and concentrations for 250 generations. Adaptation was osmolyte dependent, with sorbitol stress generally resulting in increased fitness under conditions with higher osmolarity, while selection in high concentrations of proline resulted in increased fitness specifically on proline. Consistent with these phenotypes, sequencing of the evolved populations showed that passaging in proline resulted in specific mutations in an associated metabolic pathway that increased the ability to utilize proline for growth, while evolution in sorbitol resulted in mutations in many different genes that generally resulted in improved growth under high-osmolarity conditions at the expense of growth at low osmolarity. High osmolarity decreased the growth rate but increased the mean cell volume compared with growth on proline as the sole carbon source, demonstrating that osmolarity-induced changes in growth rate and cell size follow an orthogonal relationship from the classical Growth Law relating cell size and nutrient quality. Isolates from a sorbitol-evolved population that captured the likely temporal sequence of mutations revealed by metagenomic sequencing demonstrated a trade-off between growth at high osmolarity and growth at low osmolarity. Our report highlights the utility of experimental evolution for dissecting complex cellular networks and environmental interactions, particularly in the case of behaviors that can involve both specific and general metabolic stressors. IMPORTANCE For bacteria, maintaining higher internal solute concentrations than those present in the environment allows cells to take up water. As a result, survival is challenging in high-osmolarity environments. To investigate how bacteria adapt to high-osmolarity environments, we maintained Escherichia coli in a variety of high-osmolarity solutions for hundreds of generations. We found that the evolved populations adopted different strategies to improve their growth rates depending on the osmotic passaging condition, either generally adapting to high-osmolarity conditions or better metabolizing the osmolyte as a carbon source. Single-cell imaging demonstrated that enhanced fitness was coupled to faster growth, and metagenomic sequencing revealed mutations that reflected growth trade-offs across osmolarities. Our study demonstrated the utility of long-term evolution experiments for probing adaptation occurring during environmental stress.Spencer CesarMaya Anjur-DietrichBrian YuEthan LiEnrique RojasNorma NeffTim F. CooperKerwyn Casey HuangAmerican Society for Microbiologyarticlestress responseosmotic adaptationcell morphologycell shapeprolinesorbitolMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	stress response osmotic adaptation cell morphology cell shape proline sorbitol Microbiology QR1-502
spellingShingle	stress response osmotic adaptation cell morphology cell shape proline sorbitol Microbiology QR1-502 Spencer Cesar Maya Anjur-Dietrich Brian Yu Ethan Li Enrique Rojas Norma Neff Tim F. Cooper Kerwyn Casey Huang Bacterial Evolution in High-Osmolarity Environments
description	ABSTRACT Bacteria must maintain a cytosolic osmolarity higher than that of their environment in order to take up water. High-osmolarity environments therefore present formidable stress to bacteria. To explore the evolutionary mechanisms by which bacteria adapt to high-osmolarity environments, we selected Escherichia coli in media with a variety of osmolytes and concentrations for 250 generations. Adaptation was osmolyte dependent, with sorbitol stress generally resulting in increased fitness under conditions with higher osmolarity, while selection in high concentrations of proline resulted in increased fitness specifically on proline. Consistent with these phenotypes, sequencing of the evolved populations showed that passaging in proline resulted in specific mutations in an associated metabolic pathway that increased the ability to utilize proline for growth, while evolution in sorbitol resulted in mutations in many different genes that generally resulted in improved growth under high-osmolarity conditions at the expense of growth at low osmolarity. High osmolarity decreased the growth rate but increased the mean cell volume compared with growth on proline as the sole carbon source, demonstrating that osmolarity-induced changes in growth rate and cell size follow an orthogonal relationship from the classical Growth Law relating cell size and nutrient quality. Isolates from a sorbitol-evolved population that captured the likely temporal sequence of mutations revealed by metagenomic sequencing demonstrated a trade-off between growth at high osmolarity and growth at low osmolarity. Our report highlights the utility of experimental evolution for dissecting complex cellular networks and environmental interactions, particularly in the case of behaviors that can involve both specific and general metabolic stressors. IMPORTANCE For bacteria, maintaining higher internal solute concentrations than those present in the environment allows cells to take up water. As a result, survival is challenging in high-osmolarity environments. To investigate how bacteria adapt to high-osmolarity environments, we maintained Escherichia coli in a variety of high-osmolarity solutions for hundreds of generations. We found that the evolved populations adopted different strategies to improve their growth rates depending on the osmotic passaging condition, either generally adapting to high-osmolarity conditions or better metabolizing the osmolyte as a carbon source. Single-cell imaging demonstrated that enhanced fitness was coupled to faster growth, and metagenomic sequencing revealed mutations that reflected growth trade-offs across osmolarities. Our study demonstrated the utility of long-term evolution experiments for probing adaptation occurring during environmental stress.
format	article
author	Spencer Cesar Maya Anjur-Dietrich Brian Yu Ethan Li Enrique Rojas Norma Neff Tim F. Cooper Kerwyn Casey Huang
author_facet	Spencer Cesar Maya Anjur-Dietrich Brian Yu Ethan Li Enrique Rojas Norma Neff Tim F. Cooper Kerwyn Casey Huang
author_sort	Spencer Cesar
title	Bacterial Evolution in High-Osmolarity Environments
title_short	Bacterial Evolution in High-Osmolarity Environments
title_full	Bacterial Evolution in High-Osmolarity Environments
title_fullStr	Bacterial Evolution in High-Osmolarity Environments
title_full_unstemmed	Bacterial Evolution in High-Osmolarity Environments
title_sort	bacterial evolution in high-osmolarity environments
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/774669d558a74ddf819033fab52029cf
work_keys_str_mv	AT spencercesar bacterialevolutioninhighosmolarityenvironments AT mayaanjurdietrich bacterialevolutioninhighosmolarityenvironments AT brianyu bacterialevolutioninhighosmolarityenvironments AT ethanli bacterialevolutioninhighosmolarityenvironments AT enriquerojas bacterialevolutioninhighosmolarityenvironments AT normaneff bacterialevolutioninhighosmolarityenvironments AT timfcooper bacterialevolutioninhighosmolarityenvironments AT kerwyncaseyhuang bacterialevolutioninhighosmolarityenvironments
_version_	1718427098051248128

Bacterial Evolution in High-Osmolarity Environments

Ejemplares similares