The role of division stochasticity on the robustness of bacterial size dynamics
Variables of bacterial division such as size at birth, growth rate, division time, and the position of the septal ring, all vary from cell to cell. Currently, it is unknown how these random fluctuations can combine to produce a robust mechanism of homeostasis. To address this question, we studied th...
Main Authors: | , , , , , |
---|---|
Format: | article |
Language: | Inglés |
Published: |
Cold Sprimg Harbor Laboratory (CSH)
2024
|
Subjects: | |
Online Access: | https://www.biorxiv.org/content/10.1101/2022.07.27.501776v1.article-info http://hdl.handle.net/20.500.12324/39917 https://doi.org/10.1101/2022.07.27.501776 |
id |
RepoAGROSAVIA39917 |
---|---|
record_format |
dspace |
institution |
Corporación Colombiana de Investigación Agropecuaria |
collection |
Repositorio AGROSAVIA |
language |
Inglés |
topic |
Investigación agropecuaria - A50 Bacteria Homeostasis Celdas de parición Ciclo celular Transversal http://aims.fao.org/aos/agrovoc/c_765 http://aims.fao.org/aos/agrovoc/c_33930 http://aims.fao.org/aos/agrovoc/c_2812 http://aims.fao.org/aos/agrovoc/c_37218 |
spellingShingle |
Investigación agropecuaria - A50 Bacteria Homeostasis Celdas de parición Ciclo celular Transversal http://aims.fao.org/aos/agrovoc/c_765 http://aims.fao.org/aos/agrovoc/c_33930 http://aims.fao.org/aos/agrovoc/c_2812 http://aims.fao.org/aos/agrovoc/c_37218 Nieto, César Arias Castro, Juan Carlos Sánchez, Carlos Vargas García, César Singh, Abhyudai Pedraza, Juan Manuel The role of division stochasticity on the robustness of bacterial size dynamics |
description |
Variables of bacterial division such as size at birth, growth rate, division time, and the position of the septal ring, all vary from cell to cell. Currently, it is unknown how these random fluctuations can combine to produce a robust mechanism of homeostasis. To address this question, we studied the dynamics of the cell division process from both experimental and theoretical perspectives. Our model predicts robustness in division times as sustained oscillations in metrics of the cell size distribution, such as the mean, variability, and the cell size autocorrelation function. These oscillations do not get damped, even considering stochasticity in division timing and the cell size at the beginning of the experiment. Damping appears just after inducing stochasticity in either the septum position or the growth rate. We compare the predictions of the full model with the size dynamics of E. coli bacteria growing in minimal media using either glucose or glycerol as carbon sources. We observe that growth in poorer media increases the noise in both partitioning position and growth rate. This additional noise results in oscillations with more damping. Although intracellular noise is known as a source of phenotypic variation, our results show that it can play a similar but subtler role in maintaining population-level homeostasis by causing rapid desynchronization of cell cycles.. |
format |
article |
author |
Nieto, César Arias Castro, Juan Carlos Sánchez, Carlos Vargas García, César Singh, Abhyudai Pedraza, Juan Manuel |
author_facet |
Nieto, César Arias Castro, Juan Carlos Sánchez, Carlos Vargas García, César Singh, Abhyudai Pedraza, Juan Manuel |
author_sort |
Nieto, César |
title |
The role of division stochasticity on the robustness of bacterial size dynamics |
title_short |
The role of division stochasticity on the robustness of bacterial size dynamics |
title_full |
The role of division stochasticity on the robustness of bacterial size dynamics |
title_fullStr |
The role of division stochasticity on the robustness of bacterial size dynamics |
title_full_unstemmed |
The role of division stochasticity on the robustness of bacterial size dynamics |
title_sort |
role of division stochasticity on the robustness of bacterial size dynamics |
publisher |
Cold Sprimg Harbor Laboratory (CSH) |
publishDate |
2024 |
url |
https://www.biorxiv.org/content/10.1101/2022.07.27.501776v1.article-info http://hdl.handle.net/20.500.12324/39917 https://doi.org/10.1101/2022.07.27.501776 |
work_keys_str_mv |
AT nietocesar theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT ariascastrojuancarlos theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT sanchezcarlos theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT vargasgarciacesar theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT singhabhyudai theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT pedrazajuanmanuel theroleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT nietocesar roleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT ariascastrojuancarlos roleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT sanchezcarlos roleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT vargasgarciacesar roleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT singhabhyudai roleofdivisionstochasticityontherobustnessofbacterialsizedynamics AT pedrazajuanmanuel roleofdivisionstochasticityontherobustnessofbacterialsizedynamics |
_version_ |
1842256239149449216 |
spelling |
RepoAGROSAVIA399172024-08-24T03:02:27Z The role of division stochasticity on the robustness of bacterial size dynamics The role of division stochasticity on the robustness of bacterial size dynamics Nieto, César Arias Castro, Juan Carlos Sánchez, Carlos Vargas García, César Singh, Abhyudai Pedraza, Juan Manuel Investigación agropecuaria - A50 Bacteria Homeostasis Celdas de parición Ciclo celular Transversal http://aims.fao.org/aos/agrovoc/c_765 http://aims.fao.org/aos/agrovoc/c_33930 http://aims.fao.org/aos/agrovoc/c_2812 http://aims.fao.org/aos/agrovoc/c_37218 Variables of bacterial division such as size at birth, growth rate, division time, and the position of the septal ring, all vary from cell to cell. Currently, it is unknown how these random fluctuations can combine to produce a robust mechanism of homeostasis. To address this question, we studied the dynamics of the cell division process from both experimental and theoretical perspectives. Our model predicts robustness in division times as sustained oscillations in metrics of the cell size distribution, such as the mean, variability, and the cell size autocorrelation function. These oscillations do not get damped, even considering stochasticity in division timing and the cell size at the beginning of the experiment. Damping appears just after inducing stochasticity in either the septum position or the growth rate. We compare the predictions of the full model with the size dynamics of E. coli bacteria growing in minimal media using either glucose or glycerol as carbon sources. We observe that growth in poorer media increases the noise in both partitioning position and growth rate. This additional noise results in oscillations with more damping. Although intracellular noise is known as a source of phenotypic variation, our results show that it can play a similar but subtler role in maintaining population-level homeostasis by causing rapid desynchronization of cell cycles.. 2024-08-23T15:59:21Z 2024-08-23T15:59:21Z 2022-07 2022 article Artículo científico http://purl.org/coar/resource_type/c_2df8fbb1 info:eu-repo/semantics/article https://purl.org/redcol/resource_type/ART http://purl.org/coar/version/c_970fb48d4fbd8a85 https://www.biorxiv.org/content/10.1101/2022.07.27.501776v1.article-info http://hdl.handle.net/20.500.12324/39917 https://doi.org/10.1101/2022.07.27.501776 reponame:Biblioteca Digital Agropecuaria de Colombia instname:Corporación colombiana de investigación agropecuaria AGROSAVIA eng BioRxiv 1 1 11 Y.-M. Zhang and C. O. Rock, “Membrane lipid homeostasis in bacteria,” Nature Reviews Microbiology, vol. 6, no. 3, pp. 222–233, 2008. N. Demaurex, “ph homeostasis of cellular organelles,” Physiology, vol. 17, no. 1, pp. 1–5, 2002. H. Kempe, A. Schwabe, F. Crémazy, P. J. Verschure, and F. J. Bruggeman, “The volumes and transcript counts of single cells reveal concentration homeostasis and capture biological noise,” Molecular biology of the cell, vol. 26, no. 4, pp. 797–804, 2015. J. Lin and A. Amir, “Homeostasis of protein and mrna concentrations in growing cells,” Nature communications, vol. 9, no. 1, pp. 1– 11, 2018. C. A. Vargas-Garcia, K. R. Ghusinga, and A. Singh, “Cell size control and gene expression homeostasis in single-cells,” Current opinion in systems biology, vol. 8, pp. 109–116, 2018. P. A. Levin and S. Taheri-Araghi, “One is nothing without the other: theoretical and empirical analysis of cell growth and cell cycle progression,” Journal of molecular biology, vol. 431, no. 11, pp. 2061– 2067, 2019. S. Jun, F. Si, R. Pugatch, and M. Scott, “Fundamental principles in bacterial physiology—history, recent progress, and the future with focus on cell size control: a review,” Reports on Progress in Physics, vol. 81, no. 5, p. 056601, 2018. F. Si, G. Le Treut, J. T. Sauls, S. Vadia, P. A. Levin, and S. Jun, “Mechanistic origin of cell-size control and homeostasis in bacteria,” Current Biology, vol. 29, no. 11, pp. 1760–1770, 2019. C. Nieto, C. Vargas-Garcia, and J. M. Pedraza, “Continuous rate modeling of bacterial stochastic size dynamics,” Physical Review E, vol. 104, no. 4, p. 044415, 2021. P. Bokes and A. Singh, “Cell volume distributions in exponentially growing populations,” in International Conference on Computational Methods in Systems Biology, pp. 140–154, Springer, 2019. D. Huh and J. Paulsson, “Random partitioning of molecules at cell division,” Proceedings of the National Academy of Sciences, vol. 108, no. 36, pp. 15004–15009, 2011. M. Soltani, C. A. Vargas-Garcia, D. Antunes, and A. Singh, “Intercellular variability in protein levels from stochastic expression and noisy cell cycle processes,” PLoS computational biology, vol. 12, no. 8, p. e1004972, 2016. N. Nordholt, J. Van Heerden, R. Kort, and F. J. Bruggeman, “Effects of growth rate and promoter activity on single-cell protein expression,” Scientific reports, vol. 7, no. 1, p. 6299, 2017. D. J. Kiviet, P. Nghe, N. Walker, S. Boulineau, V. Sunderlikova, and S. J. Tans, “Stochasticity of metabolism and growth at the singlecell level,” Nature, vol. 514, no. 7522, p. 376, 2014. C. Jia, A. Singh, and R. Grima, “Cell size distribution of lineage data: analytic results and parameter inference,” Iscience, vol. 24, no. 3, p. 102220, 2021. P.-Y. Ho, J. Lin, and A. Amir, “Modeling cell size regulation: From single-cell-level statistics to molecular mechanisms and population-level effects,” Annual review of biophysics, vol. 47, pp. 251–271, 2018. S. Taheri-Araghi, S. Bradde, J. T. Sauls, N. S. Hill, P. A. Levin, J. Paulsson, M. Vergassola, and S. Jun, “Cell-size control and homeostasis in bacteria,” Current Biology, vol. 25, no. 3, pp. 385– 391, 2015. C. Nieto, J. Arias-Castro, C. Sánchez, C. Vargas-García, and J. M. Pedraza, “Unification of cell division control strategies through continuous rate models,” Physical Review E, vol. 101, no. 2, p. 022401, 2020. M. Osella, E. Nugent, and M. C. Lagomarsino, “Concerted control of escherichia coli cell division,” Proceedings of the National Academy of Sciences, vol. 111, no. 9, pp. 3431–3435, 2014. P. Wang, L. Robert, J. Pelletier, W. L. Dang, F. Taddei, A. Wright, and S. Jun, “Robust growth of escherichia coli,” Current biology, vol. 20, no. 12, pp. 1099–1103, 2010. J. T. Sauls, D. Li, and S. Jun, “Adder and a coarse-grained approach to cell size homeostasis in bacteria,” Current opinion in cell biology, vol. 38, pp. 38–44, 2016. M. Priestman, P. Thomas, B. D. Robertson, and V. Shahrezaei, “Mycobacteria modify their cell size control under sub-optimal carbon sources,” Frontiers in cell and developmental biology, vol. 5, p. 64, 2017. S. Modi, C. A. Vargas-Garcia, K. R. Ghusinga, and A. Singh, “Analysis of noise mechanisms in cell-size control,” Biophysical journal, vol. 112, no. 11, pp. 2408–2418, 2017. M. Campos, I. V. Surovtsev, S. Kato, A. Paintdakhi, B. Beltran, S. E. Ebmeier, and C. Jacobs-Wagner, “A constant size extension drives bacterial cell size homeostasis,” Cell, vol. 159, no. 6, pp. 1433– 1446, 2014. C. A. Nieto-Acuna, C. A. Vargas-Garcia, A. Singh, and J. M. Pedraza, “Efficient computation of stochastic cell-size transient dynamics,” BMC bioinformatics, vol. 20, no. 23, pp. 1–6, 2019. K. R. Ghusinga, C. A. Vargas-Garcia, and A. Singh, “A mechanistic stochastic framework for regulating bacterial cell division,” Scientific reports, vol. 6, p. 30229, 2016. C. A. Vargas-García and A. Singh, “Elucidating cell size control mechanisms with stochastic hybrid systems,” in 2018 IEEE Conference on Decision and Control (CDC), pp. 4366–4371, IEEE, 2018. M. Wallden, D. Fange, E. G. Lundius, Ö. Baltekin, and J. Elf, “The synchronization of replication and division cycles in individual e. coli cells,” Cell, vol. 166, no. 3, pp. 729–739, 2016. S. Iyer-Biswas, C. S. Wright, J. T. Henry, K. Lo, S. Burov, Y. Lin, G. E. Crooks, S. Crosson, A. R. Dinner, and N. F. Scherer, “Scaling laws governing stochastic growth and division of single bacterial cells,” Proceedings of the National Academy of Sciences, vol. 111, no. 45, pp. 15912–15917, 2014. G. Micali, J. Grilli, M. Osella, and M. C. Lagomarsino, “Concurrent processes set e. coli cell division,” Science advances, vol. 4, no. 11, p. eaau3324, 2018. E. Bernard, M. Doumic, and P. Gabriel, “Cyclic asymptotic behaviour of a population reproducing by fission into two equal parts,” arXiv preprint arXiv:1609.03846, 2016. M. Kohram, H. Vashistha, S. Leibler, B. Xue, and H. Salman, “Bacterial growth control mechanisms inferred from multivariate statistical analysis of single-cell measurements,” Current Biology, vol. 31, no. 5, pp. 955–964, 2021. C. Nieto, J. Arias-Castro, C. Vargas-Garcia, C. Sanchez, and J. M. Pedraza, “Noise signature in added size suggests bacteria target a commitment size to enable division,” bioRxiv, 2020. S. Klumpp, Z. Zhang, and T. Hwa, “Growth rate-dependent global effects on gene expression in bacteria,” Cell, vol. 139, no. 7, pp. 1366–1375, 2009. M. Scott, C. W. Gunderson, E. M. Mateescu, Z. Zhang, and T. Hwa, “Interdependence of cell growth and gene expression: origins and consequences,” Science, vol. 330, no. 6007, pp. 1099–1102, 2010. S. Bakshi, E. Leoncini, C. Baker, S. J. Cañas-Duarte, B. Okumus, and J. Paulsson, “Tracking bacterial lineages in complex and dynamic environments with applications for growth control and persistence,” Nature Microbiology, vol. 6, no. 6, pp. 783–791, 2021. T. Shimaya, R. Okura, Y. Wakamoto, and K. A. Takeuchi, “Scale invariance of cell size fluctuations in starving bacteria,” Communications Physics, vol. 4, no. 1, pp. 1–12, 2021. F. Büke, J. Grilli, M. C. Lagomarsino, G. Bokinsky, and S. J. Tans, “ppgpp is a bacterial cell size regulator,” Current Biology, vol. 32, no. 4, pp. 870–877, 2022. J. Marles-Wright and R. J. Lewis, “Stress responses of bacteria,” Current opinion in structural biology, vol. 17, no. 6, pp. 755–760, 2007. V. W. Rowlett and W. Margolin, “The bacterial min system,” Current biology, vol. 23, no. 13, pp. R553–R556, 2013. M. Richard and G. Yvert, “How does evolution tune biological noise?,” Frontiers in genetics, vol. 5, p. 374, 2014. J. Liu, J.-M. François, and J.-P. Capp, “Use of noise in gene expression as an experimental parameter to test phenotypic effects,” Yeast, vol. 33, no. 6, pp. 209–216, 2016. G. Witz, E. van Nimwegen, and T. Julou, “Initiation of chromosome replication controls both division and replication cycles in e. coli through a double-adder mechanism,” Elife, vol. 8, p. e48063, 2019. M. Berger and P. R. t. Wolde, “Replication initiation in e. coli is regulated via an origin-density sensor generating adder correlations,” arXiv preprint arXiv:2106.03674, 2021. H. Vashistha, M. Kohram, and H. Salman, “Non-genetic inheritance restraint of cell-to-cell variation,” Elife, vol. 10, p. e64779, 2021. J. M. Raser and E. K. O’shea, “Noise in gene expression: origins, consequences, and control,” Science, vol. 309, no. 5743, pp. 2010– 2013, 2005. M. B. Elowitz, A. J. Levine, E. D. Siggia, and P. S. Swain, “Stochastic gene expression in a single cell,” Science, vol. 297, no. 5584, pp. 1183–1186, 2002. H. Maamar, A. Raj, and D. Dubnau, “Noise in gene expression determines cell fate in bacillus subtilis,” Science, vol. 317, no. 5837, pp. 526–529, 2007. K. Lewis, “Persister cells,” Annual review of microbiology, vol. 64, pp. 357–372, 2010. J.-W. Veening, W. K. Smits, and O. P. Kuipers, “Bistability, epigenetics, and bet-hedging in bacteria,” Annu. Rev. Microbiol., vol. 62, pp. 193–210, 2008. M. ElGamel, H. Vashistha, H. Salman, and A. Mugler, “Multigenerational memory in bacterial size control,” arXiv preprint arXiv:2206.05340, 2022. A. Camilli and B. L. Bassler, “Bacterial small-molecule signaling pathways,” Science, vol. 311, no. 5764, pp. 1113–1116, 2006. Z. Vahdat, Z. Xu, and A. Singh, “Modeling protein concentrations in cycling cells using stochastic hybrid systems,” IFAC-PapersOnLine, vol. 54, no. 9, pp. 521–526, 2021. J. Jakub Jedrak, M. Kwiatkowski, and A. Ochab-Marcinek, “Exactly solvable model of gene expression in a proliferating bacterial cell population with stochastic protein bursts and protein partitioning,” Phys. Rev. E, vol. 99, p. 042416, Apr 2019. R. García-García, A. Genthon, and D. Lacoste, “Linking lineage and population observables in biological branching processes,” Phys. Rev. E, vol. 99, p. 042413, Apr 2019. P. Thomas and V. Shahrezaei, “Coordination of gene expression noise with cell size: analytical results for agent-based models of growing cell populations,” Journal of the Royal Society Interface, vol. 18, no. 178, p. 20210274, 2021. C. Nieto, “Sizedynamics,” July 2022. K. F. Jensen, “The escherichia coli k-12" wild types" w3110 and mg1655 have an rph frameshift mutation that leads to pyrimidine starvation due to low pyre expression levels.,” Journal of bacteriology, vol. 175, no. 11, pp. 3401–3407, 1993. A. Zaslaver, A. Bren, M. Ronen, S. Itzkovitz, I. Kikoin, S. Shavit, W. Liebermeister, M. G. Surette, and U. Alon, “A comprehensive library of fluorescent transcriptional reporters for escherichia coli,” Nature methods, vol. 3, no. 8, p. 623, 2006. J. H. Miller, Experiments in molecular biology. 1972. O. Samorodova and A. Samorodov, “Fast implementation of the niblack binarization algorithm for microscope image segmentation,” Pattern Recognition and Image Analysis, vol. 26, no. 3, pp. 548– 551, 2016. Attribution-NonCommercial-ShareAlike 4.0 International http://creativecommons.org/licenses/by-nc-sa/4.0/ application/pdf application/pdf Cold Sprimg Harbor Laboratory (CSH) BioRxiv; (2022): BioRxiv (July);p. 1-11. |