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Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation

BACKGROUND: Adaptive responses to nutrient limitation involve mutations that increase the efficiency of usage or uptake of the limiting nutrient. However, starvation of different nutrients has contrasting effects on physiology, resulting in different evolutionary responses. Most studies performed to...

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Autores principales: Warsi, Omar M., Andersson, Dan I., Dykhuizen, Daniel E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960147/
https://www.ncbi.nlm.nih.gov/pubmed/29776341
http://dx.doi.org/10.1186/s12862-018-1191-4
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author Warsi, Omar M.
Andersson, Dan I.
Dykhuizen, Daniel E.
author_facet Warsi, Omar M.
Andersson, Dan I.
Dykhuizen, Daniel E.
author_sort Warsi, Omar M.
collection PubMed
description BACKGROUND: Adaptive responses to nutrient limitation involve mutations that increase the efficiency of usage or uptake of the limiting nutrient. However, starvation of different nutrients has contrasting effects on physiology, resulting in different evolutionary responses. Most studies performed to understand these evolutionary responses have focused only on macronutrient limitation. Hence our understanding of adaptation under limitation of other forms of nutrients is limited. In this study, we compared the evolutionary response in populations evolving under growth-limiting conditions for a macronutrient and a major cation. RESULTS: We evolved eight populations of E. coli in nutrient-limited chemostats for 400 generations to identify the genetic basis of the mechanisms involved in efficient usage of two nutrients: nitrogen and magnesium. Our population genomic sequencing work, based on this study and previous work, allowed us to identify targets of selection under these nutrient limiting conditions. Global transcriptional regulators glnGL were targets of selection under nitrogen starvation, while proteins involved in outer-membrane biogenesis (genes from the lpt operon) were targets of selection under magnesium starvation. The protein involved in cell-cycle arrest (yhaV) was a target of selection in both environments. We re-constructed specific mutants to analyze the effect of individual mutations on fitness in nutrient limiting conditions in chemostats and in batch cultures. We further demonstrated that adaptation to nitrogen starvation proceeds via a nutrient specific mechanism, while that to magnesium starvation involves a more general mechanism. CONCLUSIONS: Our results show two different forms of adaptive strategies under limitation of nutrients that effect cellular physiology in different ways. Adaptation to nitrogen starvation proceeds by upregulation of transcriptional regulator glnG and subsequently of transporter protein amtB, both of which results in increased nitrogen scavenging ability of the cell. On the other hand, adaptation to magnesium starvation proceeds via the restructuring of the cell outer-membrane, allowing magnesium to be redistributed to other biological processes. Also, adaptation to the chemostat environment involves selection for loss of function mutations in genes that under nutrient-limiting conditions interfere with continuous growth. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1191-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-59601472018-05-24 Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation Warsi, Omar M. Andersson, Dan I. Dykhuizen, Daniel E. BMC Evol Biol Research Article BACKGROUND: Adaptive responses to nutrient limitation involve mutations that increase the efficiency of usage or uptake of the limiting nutrient. However, starvation of different nutrients has contrasting effects on physiology, resulting in different evolutionary responses. Most studies performed to understand these evolutionary responses have focused only on macronutrient limitation. Hence our understanding of adaptation under limitation of other forms of nutrients is limited. In this study, we compared the evolutionary response in populations evolving under growth-limiting conditions for a macronutrient and a major cation. RESULTS: We evolved eight populations of E. coli in nutrient-limited chemostats for 400 generations to identify the genetic basis of the mechanisms involved in efficient usage of two nutrients: nitrogen and magnesium. Our population genomic sequencing work, based on this study and previous work, allowed us to identify targets of selection under these nutrient limiting conditions. Global transcriptional regulators glnGL were targets of selection under nitrogen starvation, while proteins involved in outer-membrane biogenesis (genes from the lpt operon) were targets of selection under magnesium starvation. The protein involved in cell-cycle arrest (yhaV) was a target of selection in both environments. We re-constructed specific mutants to analyze the effect of individual mutations on fitness in nutrient limiting conditions in chemostats and in batch cultures. We further demonstrated that adaptation to nitrogen starvation proceeds via a nutrient specific mechanism, while that to magnesium starvation involves a more general mechanism. CONCLUSIONS: Our results show two different forms of adaptive strategies under limitation of nutrients that effect cellular physiology in different ways. Adaptation to nitrogen starvation proceeds by upregulation of transcriptional regulator glnG and subsequently of transporter protein amtB, both of which results in increased nitrogen scavenging ability of the cell. On the other hand, adaptation to magnesium starvation proceeds via the restructuring of the cell outer-membrane, allowing magnesium to be redistributed to other biological processes. Also, adaptation to the chemostat environment involves selection for loss of function mutations in genes that under nutrient-limiting conditions interfere with continuous growth. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-018-1191-4) contains supplementary material, which is available to authorized users. BioMed Central 2018-05-18 /pmc/articles/PMC5960147/ /pubmed/29776341 http://dx.doi.org/10.1186/s12862-018-1191-4 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Warsi, Omar M.
Andersson, Dan I.
Dykhuizen, Daniel E.
Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title_full Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title_fullStr Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title_full_unstemmed Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title_short Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
title_sort different adaptive strategies in e. coli populations evolving under macronutrient limitation and metal ion limitation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5960147/
https://www.ncbi.nlm.nih.gov/pubmed/29776341
http://dx.doi.org/10.1186/s12862-018-1191-4
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