CoChat
Sign Up
PreprintCited by 5Bacterial biofilms and quorum sensingBacterial Genetics and BiotechnologyGene Regulatory Network Analysis

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

A deterministic, c-di-GMP-dependent genetic program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis

Open access
Pérez-Burgos, María, Herfurth, Marco, Kaczmarczyk, Andreas, Harms, Andrea, Huber, Katrin, Jenal, Urs, Glatter, Timo, Søgaard-Andersen, Lotte·2024·Nature Communications
DOI 10.1101/2024.02.06.579105PMC PMC11255338

Preprint — published as 10.1038/s41467-024-50444-4

Open this paper in CoChat — free account

Abstract

Phenotypic heterogeneity in bacteria results from stochastic processes or deterministic genetic programs. These deterministic programs often incorporate the versatile second messenger c-di-GMP, and by deploying c-di-GMP metabolizing enzyme(s) asymmetrically during cell division give rise to daughter cells with different c-di-GMP levels. By contrast, less is known about how phenotypic heterogeneity is kept to a minimum. Here, we identify a deterministic c-di-GMP-dependent genetic program that is hardwired into the cell cycle of Myxococcus xanthus to minimize phenotypic heterogeneity and guarantee the formation of phenotypically similar daughter cells during division. Cells lacking the diguanylate cyclase DmxA have an aberrant motility behaviour. DmxA is recruited to the cell division site and its activity switched on during cytokinesis, resulting in a dramatic but transient increase in the c-di-GMP concentration. During cytokinesis, this c-di-GMP burst ensures the symmetric incorporation and allocation of structural motility proteins and motility regulators at the new cell poles of the two daughters, thereby generating mirror-symmetric, phenotypically similar daughters with correct motility behaviours. These findings suggest a general c-di-GMP-dependent mechanism for minimizing phenotypic heterogeneity, and demonstrate that bacteria by deploying c-di-GMP metabolizing enzymes to distinct subcellular locations ensure the formation of dissimilar or similar daughter cells.

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 · 10.1101/2024.02.06.579105

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: 94

  1. 2022, Bacterial motility: machinery and mechanisms, Nat Rev Microbiol, 20, 161, 10.1038/s41579-021-00626-4 · DOI
  2. 2017, Cyclic di-GMP: second messenger extraordinaire, Nat Rev Microbiol, 15, 271, 10.1038/nrmicro.2016.190 · DOI
  3. 10.1128/MMBR.00043-12 · DOI
  4. 10.1146/annurev-micro-012120-063427 · DOI
  5. 2023, Polarity of c-di-GMP synthesis and degradation, Microlife, 4, uqad014, 10.1093/femsml/uqad014 · DOI
  6. 2022, Spatiotemporal regulation of switching front-rear cell polarity, Curr Opin Cell Biol, 76, 102076, 10.1016/j.ceb.2022.102076 · DOI
  7. 10.3389/fmicb.2016.00781 · DOI
  8. 10.1111/j.1365-2958.2006.05095.x · DOI
  9. 10.1111/j.1365-2958.2009.06891.x · DOI
  10. 10.1128/JB.01094-13 · DOI
  11. 10.1073/pnas.1322889111 · DOI
  12. 10.1073/pnas.76.11.5952 · DOI
  13. 10.1371/journal.pgen.1005341 · DOI
  14. 10.1371/journal.pgen.1002268 · DOI
  15. 10.1126/science.1137223 · DOI
  16. 10.1073/pnas.1018556108 · DOI
  17. 10.1073/pnas.1101101108 · DOI
  18. 10.1083/jcb.201412047 · DOI
  19. 10.1016/S0960-9822(00)00705-3 · DOI
  20. 10.1073/pnas.2002783117 · DOI
  21. 10.1073/pnas.2004722117 · DOI
  22. 10.1073/pnas.82.24.8767 · DOI
  23. 10.1038/emboj.2010.114 · DOI
  24. 10.1371/journal.pbio.1000430 · DOI
  25. 10.1038/emboj.2009.356 · DOI
  26. 2019, Spatial control of the GTPase MglA by localized RomR-RomX GEF and MglB GAP activities enables Myxococcus xanthus motility, Nat Microbiol, 4, 1344, 10.1038/s41564-019-0451-4 · DOI
  27. 2022, A bipartite, low-affinity roadblock domain-containing GAP complex regulates bacterial front-rear polarity, PLOS Genet, 18, e1010384, 10.1371/journal.pgen.1010384 · DOI
  28. 10.1038/sj.emboj.7601877 · DOI
  29. 2023, Molecular basis and design principles of switchable front-rear polarity and directional migration in Myxococcus xanthus, Nat Commun, 14, 4056, 10.1038/s41467-023-39773-y · DOI
  30. 10.1371/journal.pgen.1002951 · DOI
  31. 10.1371/journal.pgen.1002872 · DOI
  32. 2020, Protein-protein interaction network controlling establishment and maintenance of switchable cell polarity, PLOS Genet, 16, e1008877, 10.1371/journal.pgen.1008877 · DOI
  33. 10.1128/JB.00548-15 · DOI
  34. 2015, C-di-GMP regulates type IV pili-dependent-motility in Myxococcus xanthus, J Bacteriol, 198, 77
  35. 10.1371/journal.pgen.1006080 · DOI
  36. 10.1074/jbc.M603589200 · DOI
  37. 10.1073/pnas.0406134101 · DOI
  38. 10.1016/j.str.2013.04.026 · DOI
  39. 10.1371/journal.pbio.0060067 · DOI
  40. 10.1074/jbc.M704702200 · DOI
  41. 2020, CdbA is a DNA-binding protein and c-di-GMP receptor important for nucleoid organization and segregation in Myxococcus xanthus, Nat Commun, 11, 1791, 10.1038/s41467-020-15628-8 · DOI
  42. 10.1016/j.str.2009.07.019 · DOI
  43. 10.1111/j.1365-2958.1995.mmi_18030547.x · DOI
  44. 10.1111/j.1365-2958.2004.04221.x · DOI
  45. 10.1111/mmi.12094 · DOI
  46. 10.1016/j.devcel.2017.04.011 · DOI
  47. Kaczmarczyk, A. et al. A novel biosensor reveals dynamic changes of c-di-GMP in differentiating cells with ultra-high temporal resolution. bioRxiv, 2022.2010.2018.512705 (2022). · DOI
  48. 2023, The mechanism for polar localization of the type IVa pilus machine in Myxococcus xanthus, mBio, 14, e0159323, 10.1128/mbio.01593-23 · DOI
  49. 10.1126/science.aad2001 · DOI
  50. 10.1128/JB.01793-07 · DOI
  51. 10.1073/pnas.2115061119 · DOI
  52. 10.1101/gad.289504 · DOI
  53. 10.1016/j.molcel.2011.07.018 · DOI
  54. 10.7554/eLife.01402 · DOI
  55. Rick, T. et al. GGDEF domain as spatial on-switch for a phosphodiesterase by interaction with landmark protein HubP. NPJ Biofilms Microbiomes 8, 35 (2022). · DOI
  56. 10.1371/journal.pgen.1003744 · DOI
  57. 10.1126/science.1188658 · DOI
  58. 10.1016/j.chom.2018.11.008 · DOI
  59. 10.7554/eLife.45084 · DOI
  60. 10.1038/nrmicro1381 · DOI
  61. 10.1146/annurev.micro.62.081307.163002 · DOI
  62. 10.1038/nrmicro3491 · DOI
  63. 10.1128/MMBR.00040-09 · DOI
  64. 10.1073/pnas.74.7.2938 · DOI
  65. 10.1128/JB.01502-07 · DOI
  66. 10.1073/pnas.90.8.3378 · DOI
  67. 10.1038/nmeth.2019 · DOI · Paper page
  68. Sambrook, J. & Russell, D.W. Molecular Cloning: A Laboratory Manual, Edn. 3rd. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.; 2001).
  69. 10.1038/s41467-020-18803-z · DOI
  70. 10.1038/s41592-022-01639-4 · DOI
  71. 10.1111/mmi.13264 · DOI
  72. Schumacher, D. & Søgaard-Andersen, L . Fluorescence live-cell imaging of the complete vegetative cell cycle of the slow-growing social bacterium Myxococcus xanthus . J Vis Exp (2018). · DOI
  73. 10.1007/978-1-62703-245-2_6 · DOI
  74. 10.1016/j.mimet.2010.03.020 · DOI
  75. 10.1007/978-1-62703-691-7_2 · DOI · Paper page
  76. 10.1007/978-1-4939-7240-1_7 · DOI
  77. 10.1002/0471140864.ps1925s79 · DOI
  78. 2023, A miniTurbo-based proximity labeling protocol to identify conditional protein interactomes in vivo in Myxococcus xanthus, STAR Protoc, 4, 102657, 10.1016/j.xpro.2023.102657 · DOI
  79. 10.1038/nbt.4201 · DOI · Paper page
  80. 10.1093/nar/gky1049 · DOI · Paper page
  81. 10.1021/pr300273g · DOI
  82. 2022, Evidence for a widespread third system for bacterial polysaccharide export across the outer membrane comprising a composite OPX/beta-barrel translocon, mBio, 13, e0203222, 10.1128/mbio.02032-22 · DOI
  83. 2020, DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput, Nat Methods, 17, 41, 10.1038/s41592-019-0638-x · DOI
  84. 10.1093/nar/gkac1040 · DOI
  85. 10.1093/NAR/GKAB1038 · DOI · Paper page
  86. 10.1093/nar/28.1.27 · DOI · Paper page
  87. 10.1093/nar/gkaa977 · DOI · Paper page
  88. 10.1093/nar/gku949 · DOI
  89. Evans, R. , et al. Protein complex prediction with AlphaFold-Multimer. bioRxiv, 2021.2010.2004.463034 (2022).
  90. 10.1038/S41592-022-01488-1 · DOI · Paper page
  91. 10.1093/molbev/msw054 · DOI
  92. 10.1093/oxfordjournals.molbev.a040454 · DOI
  93. 10.2307/2408678 · DOI
  94. 2021, CRP-like transcriptional regulator MrpC curbs c-di-GMP and 3’,3’-cGAMP nucleotide levels during development in Myxococcus xanthus, mBio, 13, e0004422

Metadata

Authors
Pérez-Burgos, M., Herfurth, M., Kaczmarczyk, A., Harms, A., Huber, K., Jenal, U., Glatter, T., & Søgaard-Andersen, L.
Affiliations
  • Max Planck Institute for Terrestrial Microbiology (DE)
  • University of Basel (CH)
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2024-02-06
Volume
15
Issue
1
Pages
6014-6014
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2024.02.06.579105
PMC
PMC11255338
OpenAlex
W4400735943
Cited by
5
References
1
Citations by year
2026: 1 · 2025: 3 · 2024: 1
FWCI
0.68
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Science Foundation
  • Deutsche Forschungsgemeinschaft (SFB987)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (208107, 310030)
  • Max-Planck-Gesellschaft
  • Medizinischen Hochschule Hannover
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
c-di-GMP, phenotypic heterogeneity, Myxococcus xanthus, cytokinesis, diguanylate cyclase, cell division, motility, second messenger signaling, cell cycle regulation
MeSH terms
Bacterial Proteins, Cell Division, Cyclic GMP, Phenotype, Gene Expression Regulation, Bacterial, Myxococcus xanthus, Phosphorus-Oxygen Lyases, Escherichia coli Proteins, Cytokinesis

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