Analysis of Factors Limiting Bacterial Growth in PDMS Mother Machine Devices

Yang, Da; Jennings, Anna D.; Borrego, Evalynn; Retterer, Scott T.; Mannik, Jaan

doi:10.3389/fmicb.2018.00871

Title: Analysis of Factors Limiting Bacterial Growth in PDMS Mother Machine Devices

Journal Article · Tue May 01 00:00:00 EDT 2018 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2018.00871· OSTI ID:1436023

Yang, Da ^[1]; Jennings, Anna D. ^[1]; Borrego, Evalynn ^[2];

^[3]; Mannik, Jaan ^[1]

The Univ. of Tennessee, Knoxville, TN (United States)
Univ. of Tennessee, Knoxville, TN (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

The microfluidic mother machine platform has attracted much interest for its potential in studies of bacterial physiology, cellular organization, and cell mechanics. Despite numerous experiments and development of dedicated analysis software, differences in bacterial growth and morphology in narrow mother machine channels compared to typical liquid media conditions have not been systematically characterized. Here we determine changes in E. coli growth rates and cell dimensions in different sized dead-end microfluidic channels using high resolution optical microscopy. We find that E. coli adapt to the confined channel environment by becoming narrower and longer compared to the same strain grown in liquid culture. Cell dimensions decrease as the channel length increases and width decreases. These changes are accompanied by increases in doubling times in agreement with the universal growth law. In channels 100 μm and longer, cell doublings can completely stop as a result of frictional forces that oppose cell elongation. Before complete cessation of elongation, mechanical stresses lead to substantial deformation of cells and changes in their morphology. Lastly, our work shows that mechanical forces rather than nutrient limitation are the main growth limiting factor for bacterial growth in long and narrow channels.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1436023

Journal Information:: Frontiers in Microbiology, Vol. 9; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 35 works

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References (42)

High-throughput gene expression analysis at the level of single proteins using a microfluidic turbidostat and automated cell tracking Ullman, G.; Wallden, M.; Marklund, E. G. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1611 https://doi.org/10.1098/rstb.2012.0025	journal	February 2013
Chromosome replication and the division cycle of Escherichia coli Cooper, Stephen; Helmstetter, Charles E. Journal of Molecular Biology, Vol. 31, Issue 3 https://doi.org/10.1016/0022-2836(68)90425-7	journal	February 1968
Use of a microfluidic platform to uncover basic features of energy and environmental stress responses in individual cells of Bacillus subtilis Cabeen, Matthew T.; Russell, Jonathan R.; Paulsson, Johan PLOS Genetics, Vol. 13, Issue 7 https://doi.org/10.1371/journal.pgen.1006901	journal	July 2017
From the regulation of peptidoglycan synthesis to bacterial growth and morphology Typas, Athanasios; Banzhaf, Manuel; Gross, Carol A. Nature Reviews Microbiology, Vol. 10, Issue 2 https://doi.org/10.1038/nrmicro2677	journal	December 2011
Multi-color imaging of the bacterial nucleoid and division proteins with blue, orange, and near-infrared fluorescent proteins Wu, Fabai; Van Rijn, Erwin; Van Schie, Bas G. C. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00607	journal	June 2015
Sizing up the bacterial cell cycle Willis, Lisa; Huang, Kerwyn Casey Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.79	journal	August 2017
Robustness and accuracy of cell division in Escherichia coli in diverse cell shapes Mannik, J.; Wu, F.; Hol, F. J. H. Proceedings of the National Academy of Sciences, Vol. 109, Issue 18 https://doi.org/10.1073/pnas.1120854109	journal	April 2012
Stochasticity and homeostasis in the E. coli replication and division cycle Adiciptaningrum, Aileen; Osella, Matteo; Moolman, M. Charl Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep18261	journal	December 2015
Diffusion Measurements, at 25°, of Aqueous Solutions of Amino Acids, Peptides and Sugars Longsworth, L. G. Journal of the American Chemical Society, Vol. 75, Issue 22 https://doi.org/10.1021/ja01118a065	journal	November 1953
Image-Based Single Cell Profiling: High-Throughput Processing of Mother Machine Experiments Sachs, Christian Carsten; Grünberger, Alexander; Helfrich, Stefan PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0163453	journal	September 2016
Dependency on Medium and Temperature of Cell Size and Chemical Composition during Balanced Growth of Salmonella typhimurium Schaechter, M.; MaalOe, O.; Kjeldgaard, N. O. Journal of General Microbiology, Vol. 19, Issue 3 https://doi.org/10.1099/00221287-19-3-592	journal	December 1958
Evidence for Divisome Localization Mechanisms Independent of the Min System and SlmA in Escherichia coli Bailey, Matthew W.; Bisicchia, Paola; Warren, Boyd T. PLoS Genetics, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pgen.1004504	journal	August 2014
Bacterial growth and motility in sub-micron constrictions Mannik, J.; Driessen, R.; Galajda, P. Proceedings of the National Academy of Sciences, Vol. 106, Issue 35 https://doi.org/10.1073/pnas.0907542106	journal	August 2009
Microfabrication meets microbiology Weibel, Douglas B.; DiLuzio, Willow R.; Whitesides, George M. Nature Reviews Microbiology, Vol. 5, Issue 3 https://doi.org/10.1038/nrmicro1616	journal	March 2007
Microfluidic chemostat for measuring single cell dynamics in bacteria Long, Zhicheng; Nugent, Eileen; Javer, Avelino Lab on a Chip, Vol. 13, Issue 5 https://doi.org/10.1039/c2lc41196b	journal	January 2013
Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity: Measuring cellular mechanical properties with hydrogels Tuson, Hannah H.; Auer, George K.; Renner, Lars D. Molecular Microbiology, Vol. 84, Issue 5 https://doi.org/10.1111/j.1365-2958.2012.08063.x	journal	May 2012
On the location error of curved edges in low-pass filtered 2-D and 3-D images Verbeek, P. W.; van Vliet, L. J. IEEE Transactions on Pattern Analysis and Machine Intelligence, Vol. 16, Issue 7 https://doi.org/10.1109/34.297954	journal	July 1994
Memory and modularity in cell-fate decision making Norman, Thomas M.; Lord, Nathan D.; Paulsson, Johan Nature, Vol. 503, Issue 7477 https://doi.org/10.1038/nature12804	journal	November 2013
Monitoring single-cell gene regulation under dynamically controllable conditions with integrated microfluidics and software Kaiser, Matthias; Jug, Florian; Julou, Thomas Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-017-02505-0	journal	January 2018
Kinetics of large-scale chromosomal movement during asymmetric cell division in Escherichia coli Männik, Jaana; Bailey, Matthew W.; O’Neill, Jordan C. PLOS Genetics, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pgen.1006638	journal	February 2017
Antibiotic susceptibility testing in less than 30 min using direct single-cell imaging Baltekin, Özden; Boucharin, Alexis; Tano, Eva Proceedings of the National Academy of Sciences, Vol. 114, Issue 34 https://doi.org/10.1073/pnas.1708558114	journal	August 2017
Zooming in to see the bigger picture: Microfluidic and nanofabrication tools to study bacteria Hol, Felix J. H.; Dekker, Cees Science, Vol. 346, Issue 6208 https://doi.org/10.1126/science.1251821	journal	October 2014
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Datsenko, K. A.; Wanner, B. L. Proceedings of the National Academy of Sciences, Vol. 97, Issue 12, p. 6640-6645 https://doi.org/10.1073/pnas.120163297	journal	May 2000
Bending forces plastically deform growing bacterial cell walls Amir, A.; Babaeipour, F.; McIntosh, D. B. Proceedings of the National Academy of Sciences, Vol. 111, Issue 16 https://doi.org/10.1073/pnas.1317497111	journal	April 2014
Mechanical Forces of Fission Yeast Growth Minc, Nicolas; Boudaoud, Arezki; Chang, Fred Current Biology, Vol. 19, Issue 13 https://doi.org/10.1016/j.cub.2009.05.031	journal	July 2009
Robust Growth of Escherichia coli Wang, Ping; Robert, Lydia; Pelletier, James Current Biology, Vol. 20, Issue 12 https://doi.org/10.1016/j.cub.2010.04.045	journal	June 2010
A Constant Size Extension Drives Bacterial Cell Size Homeostasis Campos, Manuel; Surovtsev, Ivan V.; Kato, Setsu Cell, Vol. 159, Issue 6 https://doi.org/10.1016/j.cell.2014.11.022	journal	December 2014
Cell-Size Control and Homeostasis in Bacteria Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T. Current Biology, Vol. 25, Issue 3 https://doi.org/10.1016/j.cub.2014.12.009	journal	February 2015
Dynamics of Glucose Uptake by Single Escherichia coli Cells Natarajan, Arvind; Srienc, Friedrich Metabolic Engineering, Vol. 1, Issue 4 https://doi.org/10.1006/mben.1999.0125	journal	October 1999
Bacterial Colonies in Solid Media and Foods: A Review on Their Growth and Interactions with the Micro-Environment Jeanson, Sophie; Floury, Juliane; Gagnaire, Valérie Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01284	journal	December 2015
Permeation-driven flow in poly(dimethylsiloxane) microfluidic devices Randall, G. C.; Doyle, P. S. Proceedings of the National Academy of Sciences, Vol. 102, Issue 31, p. 10813-10818 https://doi.org/10.1073/pnas.0503287102	journal	July 2005
Characterization of small microfluidic valves for studies of mechanical properties of bacteria Yang, Da; Greer, Clayton M.; Jones, Branndon P. Journal of Vacuum Science & Technology B, Nanotechnology and Microelectronics: Materials, Processing, Measurement, and Phenomena, Vol. 33, Issue 6 https://doi.org/10.1116/1.4929883	journal	November 2015
The single-cell chemostat: an agarose-based, microfluidic device for high-throughput, single-cell studies of bacteria and bacterial communities Moffitt, Jeffrey R.; Lee, Jeffrey B.; Cluzel, Philippe Lab on a Chip, Vol. 12, Issue 8 https://doi.org/10.1039/c2lc00009a	journal	January 2012
Chromosome Replication and the Division Cycle of Escherichia coli B/r Kubitschek, H. E.; Freedman, M. L. Journal of Bacteriology, Vol. 107, Issue 1 https://doi.org/10.1128/JB.107.1.95-99.1971	journal	July 1971
Monitoring single-cell gene regulation under dynamically controllable conditions with integrated microfluidics and software Kaiser, Matthias; Jug, Florian; Julou, Thomas Nature Publishing Group https://doi.org/10.5451/unibas-ep59178	text	January 2018
Cell-Size Control and Homeostasis in Bacteria Taheri-Araghi, Sattar; Bradde, Serena; Sauls, John T. Current Biology, Vol. 27, Issue 9 https://doi.org/10.1016/j.cub.2017.04.028	journal	May 2017
Hi-throughput gene expression analysis at the level of single proteins using a microfluidic turbidostat and automated cell tracking Ullman, G.; Wallden, M.; Marklund, E. G. arXiv https://doi.org/10.48550/arxiv.1207.4048	preprint	January 2012
Bending forces plastically deform growing bacterial cell walls Amir, Ariel; Babaeipour, Farinaz; McIntosh, Dustin B. arXiv https://doi.org/10.48550/arxiv.1305.5843	text	January 2013
Quantitative and qualitative microscale distribution of bacteria in soil Ranjard, Lionel; Richaume, Agnès Research in Microbiology, Vol. 152, Issue 8 https://doi.org/10.1016/s0923-2508(01)01251-7	journal	October 2001
Design of stable and self-regulated microbial consortia for chemical synthesis Li, Xianglai; Zhou, Zhao; Li, Wenna Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29215-6	journal	March 2022
Nutrient shielding in clusters of cells Lavrentovich, Maxim O.; Koschwanez, John H.; Nelson, David R. Physical Review E, Vol. 87, Issue 6 https://doi.org/10.1103/physreve.87.062703	journal	June 2013
Effect of Nutrient Concentration on the Growth of Escherichia coli Shehata, Talaat E.; Marr, Allen G. Journal of Bacteriology, Vol. 107, Issue 1 https://doi.org/10.1128/jb.107.1.210-216.1971	journal	January 1971

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Microbial single-cell growth response at defined carbon limiting conditions Lindemann, Dorina; Westerwalbesloh, Christoph; Kohlheyer, Dietrich RSC Advances, Vol. 9, Issue 25 https://doi.org/10.1039/c9ra02454a	journal	January 2019
Cell cycle-dependent regulation of FtsZ in Escherichia coli in slow growth conditions: Cell cycle-dependent regulation of FtsZ in Escherichia coli Männik, Jaana; Walker, Bryant E.; Männik, Jaan Molecular Microbiology, Vol. 110, Issue 6 https://doi.org/10.1111/mmi.14135	journal	October 2018
The effects of polydisperse crowders on the compaction of the Escherichia coli nucleoid Yang, Da; Männik, Jaana; Retterer, Scott T. Molecular Microbiology, Vol. 113, Issue 5 https://doi.org/10.1111/mmi.14467	journal	February 2020
Microbial single-cell growth response at defined carbon limiting conditions Lindemann, Dorina; Westerwalbesloh, Christoph; Kohlheyer, Dietrich RWTH Aachen University https://doi.org/10.18154/rwth-2019-05589	text	January 2019
Metabolic activity affects response of single cells to a nutrient switch in structured populations Dal Co, Alma; Ackermann, Martin; Van Vliet, Simon The University of British Columbia https://doi.org/10.14288/1.0380994	text	January 2019
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59 BASIC BIOLOGICAL SCIENCES
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Title: Analysis of Factors Limiting Bacterial Growth in PDMS Mother Machine Devices

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