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...
Main Authors: | , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2021-11-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/69019 |
_version_ | 1811200737454063616 |
---|---|
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. |
first_indexed | 2024-04-12T02:08:45Z |
format | Article |
id | doaj.art-3631e860f20c479ab63f583005d0297c |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-12T02:08:45Z |
publishDate | 2021-11-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT michaeljahn proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT nickcrang proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT markusjanasch proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT andreashober proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT bjornforsstrom proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT kylekimler proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT alexandermattausch proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT qichen proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT johannesasplundsamuelsson proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator AT eltonpaulhudson proteinallocationandutilizationintheversatilechemolithoautotrophcupriavidusnecator |