Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator

Bacteria must balance the different needs for substrate assimilation, growth functions, and resilience in order to thrive in their environment. Of all cellular macromolecules, the bacterial proteome is by far the most important resource and its size is limited. Here, we investigated how the highly v...

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Main Authors: Michael Jahn, Nick Crang, Markus Janasch, Andreas Hober, Björn Forsström, Kyle Kimler, Alexander Mattausch, Qi Chen, Johannes Asplund-Samuelsson, Elton Paul Hudson
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/69019
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author Michael Jahn
Nick Crang
Markus Janasch
Andreas Hober
Björn Forsström
Kyle Kimler
Alexander Mattausch
Qi Chen
Johannes Asplund-Samuelsson
Elton Paul Hudson
author_facet Michael Jahn
Nick Crang
Markus Janasch
Andreas Hober
Björn Forsström
Kyle Kimler
Alexander Mattausch
Qi Chen
Johannes Asplund-Samuelsson
Elton Paul Hudson
author_sort Michael Jahn
collection DOAJ
description Bacteria must balance the different needs for substrate assimilation, growth functions, and resilience in order to thrive in their environment. Of all cellular macromolecules, the bacterial proteome is by far the most important resource and its size is limited. Here, we investigated how the highly versatile 'knallgas' bacterium Cupriavidus necator reallocates protein resources when grown on different limiting substrates and with different growth rates. We determined protein quantity by mass spectrometry and estimated enzyme utilization by resource balance analysis modeling. We found that C. necator invests a large fraction of its proteome in functions that are hardly utilized. Of the enzymes that are utilized, many are present in excess abundance. One prominent example is the strong expression of CBB cycle genes such as Rubisco during growth on fructose. Modeling and mutant competition experiments suggest that CO2-reassimilation through Rubisco does not provide a fitness benefit for heterotrophic growth, but is rather an investment in readiness for autotrophy.
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spelling doaj.art-3631e860f20c479ab63f583005d0297c2022-12-22T03:52:27ZengeLife Sciences Publications LtdeLife2050-084X2021-11-011010.7554/eLife.69019Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necatorMichael Jahn0https://orcid.org/0000-0002-3913-153XNick Crang1https://orcid.org/0000-0002-7569-6597Markus Janasch2https://orcid.org/0000-0001-7745-720XAndreas Hober3https://orcid.org/0000-0001-8947-2562Björn Forsström4https://orcid.org/0000-0002-5248-8568Kyle Kimler5Alexander Mattausch6Qi Chen7Johannes Asplund-Samuelsson8https://orcid.org/0000-0001-8077-5305Elton Paul Hudson9https://orcid.org/0000-0003-1899-7649School of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenSchool of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH – Royal Institute of Technology, Stockholm, SwedenBacteria must balance the different needs for substrate assimilation, growth functions, and resilience in order to thrive in their environment. Of all cellular macromolecules, the bacterial proteome is by far the most important resource and its size is limited. Here, we investigated how the highly versatile 'knallgas' bacterium Cupriavidus necator reallocates protein resources when grown on different limiting substrates and with different growth rates. We determined protein quantity by mass spectrometry and estimated enzyme utilization by resource balance analysis modeling. We found that C. necator invests a large fraction of its proteome in functions that are hardly utilized. Of the enzymes that are utilized, many are present in excess abundance. One prominent example is the strong expression of CBB cycle genes such as Rubisco during growth on fructose. Modeling and mutant competition experiments suggest that CO2-reassimilation through Rubisco does not provide a fitness benefit for heterotrophic growth, but is rather an investment in readiness for autotrophy.https://elifesciences.org/articles/69019Cupriavidus necatorRalstonia eutropharesource balance analysissubstrate limitationco2 fixationgene fitness
spellingShingle Michael Jahn
Nick Crang
Markus Janasch
Andreas Hober
Björn Forsström
Kyle Kimler
Alexander Mattausch
Qi Chen
Johannes Asplund-Samuelsson
Elton Paul Hudson
Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
eLife
Cupriavidus necator
Ralstonia eutropha
resource balance analysis
substrate limitation
co2 fixation
gene fitness
title Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
title_full Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
title_fullStr Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
title_full_unstemmed Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
title_short Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
title_sort protein allocation and utilization in the versatile chemolithoautotroph cupriavidus necator
topic Cupriavidus necator
Ralstonia eutropha
resource balance analysis
substrate limitation
co2 fixation
gene fitness
url https://elifesciences.org/articles/69019
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