Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli

Understanding how cells grow and adapt under various nutrient conditions is pivotal in the study of biological stoichiometry. Recent studies provide empirical evidence that cells use multiple strategies to maintain an optimal protein production rate under different nutrient conditions. Mathematical...

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Main Authors: Tin Phan, Changhan He, Irakli Loladze, Clay Prater, Jim Elser, Yang Kuang
Format: Article
Language:English
Published: Elsevier 2022-07-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844022011082
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author Tin Phan
Changhan He
Irakli Loladze
Clay Prater
Jim Elser
Yang Kuang
author_facet Tin Phan
Changhan He
Irakli Loladze
Clay Prater
Jim Elser
Yang Kuang
author_sort Tin Phan
collection DOAJ
description Understanding how cells grow and adapt under various nutrient conditions is pivotal in the study of biological stoichiometry. Recent studies provide empirical evidence that cells use multiple strategies to maintain an optimal protein production rate under different nutrient conditions. Mathematical models can provide a solid theoretical foundation that can explain experimental observations and generate testable hypotheses to further our understanding of the growth process. In this study, we generalize a modeling framework that centers on the translation process and study its asymptotic behaviors to validate algebraic manipulations involving the steady states. Using experimental results on the growth of E. coli under C-, N-, and P-limited environments, we simulate the expected quantitative measurements to show the feasibility of using the model to explain empirical evidence. Our results support the findings that cells employ multiple strategies to maintain a similar protein production rate across different nutrient limitations. Moreover, we find that the previous study underestimates the significance of certain biological rates, such as the binding rate of ribosomes to mRNA and the transition rate between different ribosomal stages. Furthermore, our simulation shows that the strategies used by cells under C- and P-limitations result in a faster overall growth dynamics than under N-limitation. In conclusion, the general modeling framework provides a valuable platform to study cell growth under different nutrient supply conditions, which also allows straightforward extensions to the coupling of transcription, translation, and energetics to deepen our understanding of the growth process.
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spelling doaj.art-25e8682a53504a2095e16178a83513e82022-12-22T03:40:56ZengElsevierHeliyon2405-84402022-07-0187e09820Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coliTin Phan0Changhan He1Irakli Loladze2Clay Prater3Jim Elser4Yang Kuang5School of Mathematical and Statistical Sciences, Arizona State University, Tempe, AZ 85287, USA; Division of Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87544, USASchool of Mathematical and Statistical Sciences, Arizona State University, Tempe, AZ 85287, USABryan Medical Center, Bryan College of Health Sciences, Lincoln, NE 68506, USADepartment of Integrative Biology, Oklahoma State University, Stillwater, OK 74078, USAFlathead Lake Bio Station, University of Montana, Polson, MT 59860, USASchool of Mathematical and Statistical Sciences, Arizona State University, Tempe, AZ 85287, USA; Corresponding author.Understanding how cells grow and adapt under various nutrient conditions is pivotal in the study of biological stoichiometry. Recent studies provide empirical evidence that cells use multiple strategies to maintain an optimal protein production rate under different nutrient conditions. Mathematical models can provide a solid theoretical foundation that can explain experimental observations and generate testable hypotheses to further our understanding of the growth process. In this study, we generalize a modeling framework that centers on the translation process and study its asymptotic behaviors to validate algebraic manipulations involving the steady states. Using experimental results on the growth of E. coli under C-, N-, and P-limited environments, we simulate the expected quantitative measurements to show the feasibility of using the model to explain empirical evidence. Our results support the findings that cells employ multiple strategies to maintain a similar protein production rate across different nutrient limitations. Moreover, we find that the previous study underestimates the significance of certain biological rates, such as the binding rate of ribosomes to mRNA and the transition rate between different ribosomal stages. Furthermore, our simulation shows that the strategies used by cells under C- and P-limitations result in a faster overall growth dynamics than under N-limitation. In conclusion, the general modeling framework provides a valuable platform to study cell growth under different nutrient supply conditions, which also allows straightforward extensions to the coupling of transcription, translation, and energetics to deepen our understanding of the growth process.http://www.sciencedirect.com/science/article/pii/S2405844022011082Inactive ribosomesModel validationGrowth rate hypothesisMathematical analysisCell growthTranslation dynamics
spellingShingle Tin Phan
Changhan He
Irakli Loladze
Clay Prater
Jim Elser
Yang Kuang
Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
Heliyon
Inactive ribosomes
Model validation
Growth rate hypothesis
Mathematical analysis
Cell growth
Translation dynamics
title Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
title_full Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
title_fullStr Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
title_full_unstemmed Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
title_short Dynamics and growth rate implications of ribosomes and mRNAs interaction in E. coli
title_sort dynamics and growth rate implications of ribosomes and mrnas interaction in e coli
topic Inactive ribosomes
Model validation
Growth rate hypothesis
Mathematical analysis
Cell growth
Translation dynamics
url http://www.sciencedirect.com/science/article/pii/S2405844022011082
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