PreprintCited by 7Microbial Metabolic Engineering and BioproductionGene Regulatory Network AnalysisBacterial Genetics and Biotechnology

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Minimization of proteome reallocation explains metabolic transition in hierarchical utilization of carbon sources

Open access

Preprint — published as 10.1128/msystems.00690-25

Abstract

Cells choose between alternative pathways in metabolic networks under diverse environmental conditions, but the principles governing the choice are insufficiently understood, especially in response to dynamically changing conditions. Here we observed that a lactic acid bacterium Bacillus coagulans displayed homolactic fermentation on glucose or trehalose as the sole carbon source, but transitioned from homolactic to heterolactic fermentation during the hierarchical utilization of glucose and trehalose when growing on the mixture. We simulated the observation by dynamic minimization of reallocation of proteome (dMORP) using an enzyme-constrained genome-scale metabolic model of B. coagulans , which coincided with our omics data. Moreover, we evolved strains to co-utilize mixed carbon sources and repress the choice of heterolactic fermentation, and the dynamics after co-utilization of carbon sources could also be captured by dMORP. Altogether, the findings suggest that upon rapid environmental changes bacteria tend to minimize proteome reallocation and accordingly adjust metabolism, and dMORP would be useful in simulating and understanding cellular dynamics.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1101/2024.01.23.576957

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 79

  1. 10.1126/science.1160809 · DOI · Paper page
  2. 10.1038/s41589-024-01571-y · DOI
  3. 10.1126/science.1058079 · DOI
  4. 10.1038/msb.2009.82 · DOI · Paper page
  5. 10.1073/pnas.1215283110 · DOI · Paper page
  6. 10.1016/j.cels.2017.06.005 · DOI
  7. 10.1073/pnas.1805367115 · DOI
  8. 10.1038/s41540-019-0093-4 · DOI
  9. 10.1038/nature15765 · DOI · Paper page
  10. 10.1073/pnas.1906569116 · DOI · Paper page
  11. 10.1126/science.1216882 · DOI · Paper page
  12. Mori M , Schink S , Erickson DW , Gerland U , Hwa T . 2017. Quantifying the benefit of a proteome reserve in fluctuating environments. Nature Communications 8. · DOI
  13. 10.1016/j.jtice.2016.01.007 · DOI
  14. 10.1002/bit.27488 · DOI
  15. 10.1016/j.cofs.2015.03.001 · DOI · Paper page
  16. 10.3389/fbioe.2021.612285 · DOI · Paper page
  17. 10.1073/pnas.1111085108 · DOI
  18. 10.1016/j.biortech.2012.11.144 · DOI
  19. 10.1016/j.biotechadv.2013.04.002 · DOI · Paper page
  20. 10.1016/j.biortech.2009.12.119 · DOI
  21. 10.15252/msb.20145537 · DOI
  22. 10.1038/s41467-020-16872-8 · DOI
  23. 10.1016/j.mib.2021.07.008 · DOI
  24. 10.1073/pnas.1320063111 · DOI
  25. 2020, Regulation underlying hierarchical and simultaneous utilization of carbon substrates by flux sensors in Escherichia coli, Nature Microbiology, 5, 206
  26. 10.1073/pnas.2013836118 · DOI
  27. 10.1073/pnas.1700345114 · DOI
  28. 10.1016/j.ymben.2013.08.003 · DOI
  29. 10.1016/j.biortech.2016.07.100 · DOI
  30. 10.1039/C5AY01703C · DOI
  31. 10.1007/BF02942348 · DOI
  32. Dooley D , Ryu S , J. Giannone R , Edwards J , S. Dien B , J. Slininger P , T. Trinh C . 2024. Expanded genome and proteome reallocation in a novel, robust Bacillus coagulans strain capable of utilizing pentose and hexose sugars. mSystems:e 00952–24. · DOI
  33. 10.1007/s00253-016-7644-z · DOI
  34. 10.1038/s41587-020-0446-y · DOI · Paper page
  35. 10.1038/s41596-023-00931-7 · DOI
  36. Alter TB , Blank LM , Ebert BE. 2021. Proteome Regulation Patterns Determine Escherichia coli Wild-Type and Mutant Phenotypes. Msystems 6. · DOI
  37. 10.1016/j.synbio.2024.04.005 · DOI
  38. 10.1002/bit.27485 · DOI · Paper page
  39. 10.1038/nbt.1614 · DOI · Paper page
  40. 2021, A multiphase multiobjective dynamic genome-scale model shows different redox balancing among yeast species of the Saccharomyces genus in fermentation. msystems, 6, 10
  41. 10.1111/1751-7915.13995 · DOI
  42. 10.1016/j.celrep.2015.12.015 · DOI
  43. Domenzain I , Sanchez B , Anton M , Kerkhoven EJ , Millan-Oropeza A , Henry C , Siewers V , Morrissey JP , Sonnenschein N , Nielsen J . 2022. Reconstruction of a catalogue of genome-scale metabolic models with enzymatic constraints using GECKO 2.0. Nature Communications 13. · DOI
  44. 10.1038/s41589-019-0364-9 · DOI
  45. 10.1016/j.biortech.2012.12.076 · DOI
  46. 10.1016/j.biortech.2019.03.057 · DOI
  47. 10.1038/srep13200 · DOI
  48. 10.3389/fcell.2023.1197226 · DOI
  49. 10.1038/s41579-022-00818-6 · DOI
  50. 10.1038/s41564-022-01310-w · DOI
  51. 10.1038/s41467-020-15749-0 · DOI
  52. 10.1186/s13059-020-02238-2 · DOI
  53. 10.1038/nature24299 · DOI
  54. 10.1038/s41586-020-2505-4 · DOI
  55. Cerulus B , Jariani A , Perez-Samper G , Vermeersch L , Pietsch JMJ , Crane MM , New AM , Gallone B , Roncoroni M , Dzialo MC , Govers SK , Hendrickx JO , Galle E , Coomans M , Berden P , Verbandt S , Swain PS , Verstrepen KJ . 2018. Transition between fermentation and respiration determines history-dependent behavior in fluctuating carbon sources. Elife 7. · DOI
  56. 10.3389/fmicb.2022.1004488 · DOI
  57. 10.1038/s41564-022-01072-5 · DOI
  58. 10.1038/s41467-017-02724-5 · DOI
  59. 10.1016/j.ymben.2021.07.001 · DOI
  60. 10.1073/pnas.232349399 · DOI
  61. 10.1371/journal.pcbi.1006302 · DOI · Paper page
  62. 10.1073/pnas.1617508114 · DOI
  63. 10.1186/s12918-018-0674-7 · DOI
  64. 10.1016/j.coisb.2021.03.003 · DOI · Paper page
  65. David AN , Sewsynker-Sukai Y , Kana EBG . 2022. Co-valorization of corn cobs and dairy wastewater for simultaneous saccharification and lactic acid production: Process optimization and kinetic assessment. Bioresource Technology 348. · DOI
  66. 10.1093/nar/28.1.27 · DOI · Paper page
  67. 10.1093/nar/30.1.59 · DOI
  68. 10.1371/journal.pcbi.1006541 · DOI · Paper page
  69. 10.1038/nbt.1672 · DOI · Paper page
  70. Aziz RK , Bartels D , Best AA , DeJongh M , Disz T , Edwards RA , Formsma K , Gerdes S , Glass EM , Kubal M , Meyer F , Olsen GJ , Olson R , Osterman AL , Overbeek RA , McNeil LK , Paarmann D , Paczian T , Parrello B , Pusch GD , Reich C , Stevens R , Vassieva O , Vonstein V , Wilke A , Zagnitko O . 2008. The RAST server: Rapid annotations using subsystems technology. Bmc Genomics 9. · DOI
  71. 10.1093/nar/gky1048 · DOI
  72. 10.1093/nar/gkac831 · DOI
  73. 10.1093/nar/gkh131 · DOI
  74. 10.1016/S0006-3495(02)73903-9 · DOI · Paper page
  75. 10.1038/s41596-018-0098-2 · DOI
  76. 10.1016/j.jbiotec.2019.04.021 · DOI
  77. 10.1007/s00449-019-02135-4 · DOI
  78. 10.3389/fmicb.2022.985465 · DOI
  79. 10.1099/13500872-140-5-1141 · DOI

Metadata

Authors
Liu, Z., Chen, M., Hu, J., Wang, Y., & Chen, Y.
Affiliations
  • East China University of Science and Technology (CN)
  • Chinese Academy of Sciences (CN)
Corresponding author
  • Wang, Yonghong
  • Chen, Yu
Venue
mSystems
Publisher
openRxiv
Published
2024-01-25
Volume
10
Issue
7
Pages
e0069025-e0069025
ISSN
2379-5077 (ISSN-L)
OpenAlex
W4411784373
Cited by
7
References
1
Citations by year
2026: 5 · 2025: 2
FWCI
2.10
Type
journal article
Language
en
Open access
Locations
  • mSystems (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (21878084)
  • National Key Research and Development Program of China (2023YFA0913900, 2024YFA0920300)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords
metabolic transition, Bacillus coagulans, homolactic fermentation, heterolactic fermentation, trehalose, glucose, mixed carbon sources, genome-scale metabolic models, lactic acid bacteria
MeSH terms
Bacillus coagulans, Bacterial Proteins, Carbon, Fermentation, Glucose, Models, Biological, Trehalose, Proteome, Metabolic Networks and Pathways

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review