skip to main content
10.1145/3459930.3469539acmconferencesArticle/Chapter ViewAbstractPublication PagesbcbConference Proceedingsconference-collections
research-article
Public Access

A spatiotemporal model of polarity and spatial gradient establishment in caulobacter crescentus

Published: 01 August 2021 Publication History

Abstract

Bacterial cells have sophisticated intracellular organization of proteins in space and time, which allows for stress response, signal transduction, cell differentiation and morphogenesis. The mechanisms of spatial localization and their contributions to cell development and adaptability are not fully understood. In this work, we use the bacterial model organism, Caulobacter cescentus, to investigate the establishment of polarity and asymmetry. We apply a reaction-diffusion model to simulating the spatiotemporal dynamics of scaffolding proteins PodJ and PopZ, which account for the formation of distinct poles in C. crescentus. Additionally, we use this mathematical model to investigate the nonuniform distribution of key kinase DivJ and phosphatase PleC and figure out their contributions to the spatial gradient of response regulators DivK and CtrA.

References

[1]
Nora Ausmees and Christine Jacobs-Wagner. 2003. Spatial and Temporal Control of Differentiation and Cell Cycle Progression in Caulobacter crescentus. Annual Review of Microbiology 57, 1: 225--247.
[2]
Manuel Campos, Ivan V Surovtsev, Setsu Kato, Ahmad Paintdakhi, Bruno Beltran, Sarah E Ebmeier, and Christine Jacobs-Wagner. 2014. A constant size extension drives bacterial cell size homeostasis. Cell 159, 6: 1433--1446.
[3]
Joseph C. Chen, Alison K. Hottes, Harley H. McAdams, Patrick T. McGrath, Patrick H. Viollier, and Lucy Shapiro. 2006. Cytokinesis signals truncation of the PodJ polarity factor by a cell cycle-regulated protease. EMBO Journal 25, 2: 377--386.
[4]
Y Erin Chen, Carolina Tropini, Kristina Jonas, Christos G Tsokos, Kerwyn C Huang, and Michael T Laub. 2011. Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium. Proceedings of the National Academy of Sciences 108, 3: 1052 LP - 1057.
[5]
Ibrahim J Domian, Kim C Quon, and Lucy Shapiro. 1997. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 3: 415--424.
[6]
Xiaoyun Guo. 2014. A bacterial scaffolding protein keeps the cell cycle and differentiation in check by regulating histidine kinase activity.
[7]
Kerwyn Casey Huang and Kumaran S Ramamurthi. 2010. Macromolecules that prefer their membranes curvy. Molecular microbiology 76, 4: 822--832.
[8]
Rasmus B Jensen, Sherry C Wang, and Lucy Shapiro. 2001. A moving DNA replication factory in Caulobacter crescentus. The EMBO journal 20, 17: 4952--4963.
[9]
Kamal Kishore Joshi, Christine M Battle, and Peter Chien. 2018. Polar localization hub protein PopZ restrains adaptor-dependent ClpXP proteolysis in Caulobacter crescentus. Journal of bacteriology 200, 20.
[10]
Kenneth C Keiler and Lucy Shapiro. 2003. tmRNA is required for correct timing of DNA replication in Caulobacter crescentus. Journal of bacteriology 185, 2: 573--580.
[11]
Shigeru Kondo and Takashi Miura. 2010. Reaction-diffusion model as a framework for understanding biological pattern formation. science 329, 5999: 1616--1620.
[12]
Kimberly Ann Kowallis. 2020. Regulatory Mechanisms of a Bacterial Multi-Kinase Network. UNIVERSITY OF PITTSBURGH.
[13]
Mohit Kumar, Mario S Mommer, and Victor Sourjik. 2010. Mobility of cytoplasmic, membrane, and DNA-binding proteins in Escherichia coli. Biophysical journal 98, 4: 552--559.
[14]
Keren Lasker, Thomas H Mann, and Lucy Shapiro. 2016. An intracellular compass spatially coordinates cell cycle modules in Caulobacter crescentus. Current Opinion in Microbiology 33: 131--139.
[15]
Keren Lasker, Jared M Schrader, Yifei Men, Tyler Marshik, David L Dill, Harley H McAdams, and Lucy Shapiro. 2016. CauloBrowser: A systems biology resource for Caulobacter crescentus. Nucleic Acids Research 44, D1: D640--D645.
[16]
Michael T Laub, Swaine L Chen, Lucy Shapiro, and Harley H McAdams. 2002. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proceedings of the National Academy of Sciences 99, 7: 4632--4637.
[17]
Melanie L Lawler, David E Larson, Aaron J Hinz, David Klein, and Yves V Brun. 2006. Dissection of functional domains of the polar localization factor PodJ in Caulobacter crescentus. Molecular microbiology 59, 1: 301--316.
[18]
Shenghua Li, Paul Brazhnik, Bruno Sobral, and John J Tyson. 2008. A quantitative study of the division cycle of Caulobacter crescentus stalked cells. PLoS computational biology 4, 1.
[19]
Shenghua Li, Paul Brazhnik, Bruno Sobral, and John J Tyson. 2009. Temporal controls of the asymmetric cell division cycle in Caulobacter crescentus. PLoS computational biology 5, 8: e1000463--e1000463.
[20]
Paula Montero Llopis, Audrey F Jackson, Oleksii Sliusarenko, Ivan Surovtsev, Jennifer Heinritz, Thierry Emonet, and Christine Jacobs-Wagner. 2010. Spatial organization of the flow of genetic information in bacteria. Nature 466, 7302: 77--81.
[21]
Seán M Murray, Gaël Panis, Coralie Fumeaux, Patrick H Viollier, and Martin Howard. 2013. Computational and genetic reduction of a cell cycle to its simplest, primordial components. PLoS Biol 11, 12: e1001749.
[22]
Adam M Perez, Thomas H Mann, Keren Lasker, Daniel G Ahrens, Michael R Eckart, and Lucy Shapiro. 2017. A localized complex of two protein oligomers controls the orientation of cell polarity. MBio 8, 1.
[23]
Francesco Pini, Benjamin Frage, Lorenzo Ferri, Nicole J De Nisco, Saswat S Mohapatra, Lucilla Taddei, Antonella Fioravanti, Frederique Dewitte, Marco Galardini, and Matteo Brilli. 2013. The DivJ, CbrA and PleC system controls DivK phosphorylation and symbiosis in S inorhizobium meliloti. Molecular microbiology 90, 1: 54--71.
[24]
Sunish Kumar Radhakrishnan, Martin Thanbichler, and Patrick H Viollier. 2008. The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes & development 22, 2: 212--225.
[25]
Lars D Renner and Douglas B Weibel. 2012. MinD and MinE interact with anionic phospholipids and regulate division plane formation in Escherichia coli. Journal of Biological Chemistry 287, 46: 38835--38844.
[26]
Kartik Subramanian, Mark R Paul, and John J Tyson. 2015. Dynamical Localization of DivL and PleC in the Asymmetric Division Cycle of Caulobacter crescentus: A Theoretical Investigation of Alternative Models. PLOS Computational Biology 11, 7: e1004348.
[27]
Kartik Subramanian and John J Tyson. 2017. Spatiotemporal models of the asymmetric division cycle of Caulobacter crescentus. Asymmetric Cell Division in Development, Differentiation and Cancer: 23--48.
[28]
Aurelio A Teleman, Peter L Graumann, Daniel Chi-Hong Lin, Alan D Grossman, and Richard Losick. 1998. Chromosome arrangement within a bacterium. Current Biology 8, 20: 1102--1109.
[29]
Benedetto Terrana and Austin Newton. 1975. Pattern of unequal cell division and development in Caulobacter crescentus. Developmental biology 44, 2: 380--385.
[30]
Carolina Tropini and Kerwyn Casey Huang. 2012. Interplay between the localization and kinetics of phosphorylation in flagellar pole development of the bacterium Caulobacter crescentus. PLoS Comput Biol 8, 8: e1002602.
[31]
Christos G Tsokos and Michael T Laub. 2012. Polarity and cell fate asymmetry in Caulobacter crescentus. Current opinion in microbiology 15, 6: 744--750.
[32]
Christos G Tsokos, Barrett S Perchuk, and Michael T Laub. 2011. A dynamic complex of signaling proteins uses polar localization to regulate cell-fate asymmetry in Caulobacter crescentus. Developmental cell 20, 3: 329--341.
[33]
Wei Zhao, Samuel W Duvall, Kimberly A Kowallis, Dylan T Tomares, Haley N Petitjean, and W Seth Childers. 2018. A circuit of protein-protein regulatory interactions enables polarity establishment in a bacterium. bioRxiv: 503250.

Cited By

View all
  • (2022)Modeling the temporal dynamics of master regulators and CtrA proteolysis in Caulobacter crescentus cell cyclePLOS Computational Biology10.1371/journal.pcbi.100984718:1(e1009847)Online publication date: 28-Jan-2022

Recommendations

Comments

Information & Contributors

Information

Published In

cover image ACM Conferences
BCB '21: Proceedings of the 12th ACM International Conference on Bioinformatics, Computational Biology, and Health Informatics
August 2021
603 pages
ISBN:9781450384506
DOI:10.1145/3459930
Permission to make digital or hard copies of all or part of this work for personal or classroom use is granted without fee provided that copies are not made or distributed for profit or commercial advantage and that copies bear this notice and the full citation on the first page. Copyrights for components of this work owned by others than the author(s) must be honored. Abstracting with credit is permitted. To copy otherwise, or republish, to post on servers or to redistribute to lists, requires prior specific permission and/or a fee. Request permissions from [email protected].

Sponsors

Publisher

Association for Computing Machinery

New York, NY, United States

Publication History

Published: 01 August 2021

Permissions

Request permissions for this article.

Check for updates

Author Tags

  1. asymmetric cell cycle
  2. reaction-diffusion model
  3. scaffolding proteins
  4. spatial gradient

Qualifiers

  • Research-article

Funding Sources

Conference

BCB '21
Sponsor:

Acceptance Rates

Overall Acceptance Rate 254 of 885 submissions, 29%

Contributors

Other Metrics

Bibliometrics & Citations

Bibliometrics

Article Metrics

  • Downloads (Last 12 months)70
  • Downloads (Last 6 weeks)11
Reflects downloads up to 03 Mar 2025

Other Metrics

Citations

Cited By

View all
  • (2022)Modeling the temporal dynamics of master regulators and CtrA proteolysis in Caulobacter crescentus cell cyclePLOS Computational Biology10.1371/journal.pcbi.100984718:1(e1009847)Online publication date: 28-Jan-2022

View Options

View options

PDF

View or Download as a PDF file.

PDF

eReader

View online with eReader.

eReader

Login options

Figures

Tables

Media

Share

Share

Share this Publication link

Share on social media