Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator

  1. Michael Jahn  Is a corresponding author
  2. Nick Crang
  3. Markus Janasch
  4. Andreas Hober
  5. Björn Forsström
  6. Kyle Kimler
  7. Alexander Mattausch
  8. Qi Chen
  9. Johannes Asplund-Samuelsson
  10. Elton Paul Hudson  Is a corresponding author
  1. Science for Life Laboratory, KTH - Royal Institute of Technology, Sweden
  2. The Broad Institute and Boston Children's Hospital, United States
  3. Heidelberg University, Germany

Abstract

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.

Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD024819. Protein quantification results can be browsed and interactively analyzed using the web application available at https://m-jahn.shinyapps.io/ShinyProt.Sequencing data for TnSeq and BarSeq experiments are available at the European Nucleotide Archive with accession number PRJEB43757. The data for competition experiments performed with the transposon mutant library can be browsed and interactively analyzed using the web application available at https://m-jahn.shinyapps.io/ShinyLib/.

The following data sets were generated

Article and author information

Author details

  1. Michael Jahn

    Nanobiotechnology, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    For correspondence
    michael.jahn@scilifelab.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3913-153X
  2. Nick Crang

    Nanobiotechnology, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7569-6597
  3. Markus Janasch

    Protein Science/Systems Biology, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7745-720X
  4. Andreas Hober

    Protein Science, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8947-2562
  5. Björn Forsström

    Systems Biology, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5248-8568
  6. Kyle Kimler

    The Broad Institute and Boston Children's Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexander Mattausch

    Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Qi Chen

    Systems Biology, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  9. Johannes Asplund-Samuelsson

    School of Engineering Sciences in Chemistry, Biotechnology and Health, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8077-5305
  10. Elton Paul Hudson

    Protein Science, Science for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden
    For correspondence
    paul.hudson@scilifelab.se
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1899-7649

Funding

Swedish Research Council Vetenskapsrådet (2016-06160)

  • Nick Crang
  • Kyle Kimler
  • Johannes Asplund-Samuelsson

Swedish Research Council Formas (2019-01491)

  • Michael Jahn

Swedish Research Council Formas (2015-939)

  • Michael Jahn

Novo Nordisk Fonden (NNF20OC0061469)

  • Markus Janasch
  • Elton Paul Hudson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gisela Storz, National Institute of Child Health and Human Development, United States

Publication history

  1. Preprint posted: March 22, 2021 (view preprint)
  2. Received: April 1, 2021
  3. Accepted: October 30, 2021
  4. Accepted Manuscript published: November 1, 2021 (version 1)
  5. Version of Record published: November 11, 2021 (version 2)
  6. Version of Record updated: November 16, 2021 (version 3)

Copyright

© 2021, Jahn et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Michael Jahn
  2. Nick Crang
  3. Markus Janasch
  4. Andreas Hober
  5. Björn Forsström
  6. Kyle Kimler
  7. Alexander Mattausch
  8. Qi Chen
  9. Johannes Asplund-Samuelsson
  10. Elton Paul Hudson
(2021)
Protein allocation and utilization in the versatile chemolithoautotroph Cupriavidus necator
eLife 10:e69019.
https://doi.org/10.7554/eLife.69019

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