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

Abstract 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 perf...

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Main Authors: Omar M. Warsi, Dan I. Andersson, Daniel E. Dykhuizen
Format: Article
Language:English
Published: BMC 2018-05-01
Series:BMC Evolutionary Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12862-018-1191-4
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spelling doaj-4c677b3064e244889aeefc9f407c16582021-09-02T15:34:30ZengBMCBMC Evolutionary Biology1471-21482018-05-0118111510.1186/s12862-018-1191-4Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitationOmar M. Warsi0Dan I. Andersson1Daniel E. Dykhuizen2Department of Ecology and Evolution, Stony Brook UniversityDepartment of Medical Biochemistry and Microbiology, Uppsala UniversityDepartment of Ecology and Evolution, Stony Brook UniversityAbstract 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.http://link.springer.com/article/10.1186/s12862-018-1191-4Nitrogen limitationMagnesium limitationExperimental evolutionLow nutrient environment
collection DOAJ
language English
format Article
sources DOAJ
author Omar M. Warsi
Dan I. Andersson
Daniel E. Dykhuizen
spellingShingle Omar M. Warsi
Dan I. Andersson
Daniel E. Dykhuizen
Different adaptive strategies in E. coli populations evolving under macronutrient limitation and metal ion limitation
BMC Evolutionary Biology
Nitrogen limitation
Magnesium limitation
Experimental evolution
Low nutrient environment
author_facet Omar M. Warsi
Dan I. Andersson
Daniel E. Dykhuizen
author_sort Omar M. Warsi
title 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_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_sort different adaptive strategies in e. coli populations evolving under macronutrient limitation and metal ion limitation
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2018-05-01
description Abstract 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.
topic Nitrogen limitation
Magnesium limitation
Experimental evolution
Low nutrient environment
url http://link.springer.com/article/10.1186/s12862-018-1191-4
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