Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation

Abstract Vibrio natriegens is a Gram‐negative bacterium with an exceptional growth rate that has the potential to become a standard biotechnological host for laboratory and industrial bioproduction. Despite this burgeoning interest, the current lack of organism‐specific qualitative and quantitative...

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Main Authors: Lucas Coppens, Tanya Tschirhart, Dagmar H Leary, Sophie M Colston, Jaimee R Compton, William Judson Hervey, Karl L Dana, Gary J Vora, Sergio Bordel, Rodrigo Ledesma‐Amaro
Format: Article
Language:English
Published: Springer Nature 2023-02-01
Series:Molecular Systems Biology
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Online Access:https://doi.org/10.15252/msb.202110523
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author Lucas Coppens
Tanya Tschirhart
Dagmar H Leary
Sophie M Colston
Jaimee R Compton
William Judson Hervey
Karl L Dana
Gary J Vora
Sergio Bordel
Rodrigo Ledesma‐Amaro
author_facet Lucas Coppens
Tanya Tschirhart
Dagmar H Leary
Sophie M Colston
Jaimee R Compton
William Judson Hervey
Karl L Dana
Gary J Vora
Sergio Bordel
Rodrigo Ledesma‐Amaro
author_sort Lucas Coppens
collection DOAJ
description Abstract Vibrio natriegens is a Gram‐negative bacterium with an exceptional growth rate that has the potential to become a standard biotechnological host for laboratory and industrial bioproduction. Despite this burgeoning interest, the current lack of organism‐specific qualitative and quantitative computational tools has hampered the community's ability to rationally engineer this bacterium. In this study, we present the first genome‐scale metabolic model (GSMM) of V. natriegens. The GSMM (iLC858) was developed using an automated draft assembly and extensive manual curation and was validated by comparing predicted yields, central metabolic fluxes, viable carbon substrates, and essential genes with empirical data. Mass spectrometry‐based proteomics data confirmed the translation of at least 76% of the enzyme‐encoding genes predicted to be expressed by the model during aerobic growth in a minimal medium. iLC858 was subsequently used to carry out a metabolic comparison between the model organism Escherichia coli and V. natriegens, leading to an analysis of the model architecture of V. natriegens' respiratory and ATP‐generating system and the discovery of a role for a sodium‐dependent oxaloacetate decarboxylase pump. The proteomics data were further used to investigate additional halophilic adaptations of V. natriegens. Finally, iLC858 was utilized to create a Resource Balance Analysis model to study the allocation of carbon resources. Taken together, the models presented provide useful computational tools to guide metabolic engineering efforts in V. natriegens.
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spelling doaj-art-20fb8d7197224a56b273f4451e2099d12025-08-20T03:46:41ZengSpringer NatureMolecular Systems Biology1744-42922023-02-0119411610.15252/msb.202110523Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocationLucas Coppens0Tanya Tschirhart1Dagmar H Leary2Sophie M Colston3Jaimee R Compton4William Judson Hervey5Karl L Dana6Gary J Vora7Sergio Bordel8Rodrigo Ledesma‐Amaro9Department of Bioengineering and Imperial College Centre for Synthetic Biology, Imperial College LondonUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringNOVA Research IncUS Naval Research Laboratory, Center for Bio/Molecular Science and EngineeringDepartment of Chemical Engineering and Environmental Technology, School of Industrial Engineering, University of ValladolidDepartment of Bioengineering and Imperial College Centre for Synthetic Biology, Imperial College LondonAbstract Vibrio natriegens is a Gram‐negative bacterium with an exceptional growth rate that has the potential to become a standard biotechnological host for laboratory and industrial bioproduction. Despite this burgeoning interest, the current lack of organism‐specific qualitative and quantitative computational tools has hampered the community's ability to rationally engineer this bacterium. In this study, we present the first genome‐scale metabolic model (GSMM) of V. natriegens. The GSMM (iLC858) was developed using an automated draft assembly and extensive manual curation and was validated by comparing predicted yields, central metabolic fluxes, viable carbon substrates, and essential genes with empirical data. Mass spectrometry‐based proteomics data confirmed the translation of at least 76% of the enzyme‐encoding genes predicted to be expressed by the model during aerobic growth in a minimal medium. iLC858 was subsequently used to carry out a metabolic comparison between the model organism Escherichia coli and V. natriegens, leading to an analysis of the model architecture of V. natriegens' respiratory and ATP‐generating system and the discovery of a role for a sodium‐dependent oxaloacetate decarboxylase pump. The proteomics data were further used to investigate additional halophilic adaptations of V. natriegens. Finally, iLC858 was utilized to create a Resource Balance Analysis model to study the allocation of carbon resources. Taken together, the models presented provide useful computational tools to guide metabolic engineering efforts in V. natriegens.https://doi.org/10.15252/msb.202110523genome‐scale metabolic modelingmetabolic engineeringresource allocationsynthetic biologyVibrio natriegens
spellingShingle Lucas Coppens
Tanya Tschirhart
Dagmar H Leary
Sophie M Colston
Jaimee R Compton
William Judson Hervey
Karl L Dana
Gary J Vora
Sergio Bordel
Rodrigo Ledesma‐Amaro
Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
Molecular Systems Biology
genome‐scale metabolic modeling
metabolic engineering
resource allocation
synthetic biology
Vibrio natriegens
title Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
title_full Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
title_fullStr Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
title_full_unstemmed Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
title_short Vibrio natriegens genome‐scale modeling reveals insights into halophilic adaptations and resource allocation
title_sort vibrio natriegens genome scale modeling reveals insights into halophilic adaptations and resource allocation
topic genome‐scale metabolic modeling
metabolic engineering
resource allocation
synthetic biology
Vibrio natriegens
url https://doi.org/10.15252/msb.202110523
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