Toward a realistic model of multilayered bacterial colonies

Authors

  • M. T. Khan Interdisciplinary Centre for Mathematical Modelling and Department of Mathematical Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, United Kingdom https://orcid.org/0009-0004-8831-7359
  • J. Cammann Interdisciplinary Centre for Mathematical Modelling and Department of Mathematical Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, United Kingdom https://orcid.org/0000-0003-3245-8078
  • A. Sengupta Physics of Living Matter Group, Department of Physics and Materials Science, University of Luxembourg, 162 A, Avenue de la Faïencerie, L-1511 Luxembourg City, Luxembourg; Institute for Advanced Studies, University of Luxembourg, 2 Avenue de l’Université, L-4365 Esch-sur-Alzette, Luxembourg https://orcid.org/0000-0001-5592-7864
  • E. Renzi Mathematics of Complex and Nonlinear Phenomena (MCNP), Department of Mathematics, Physics and Electrical Engineering, Northumbria University, Newcastle upon Tyne, NE1 8ST, United Kingdom https://orcid.org/0000-0002-1459-5565
  • M. G. Mazza Interdisciplinary Centre for Mathematical Modelling and Department of Mathematical Sciences, Loughborough University, Loughborough, Leicestershire LE11 3TU, United Kingdom https://orcid.org/0000-0002-5625-9121

DOI:

https://doi.org/10.5488/cmp.27.13802

Keywords:

bacteria, active matter, orientational order, geometry, mechanics, mono-to-multilayer transition

Abstract

Bacteria are prolific at colonizing diverse surfaces under a widerange of environmental conditions, and exhibit fascinating examples of self-organization across scales. Though it has recently attracted considerable interest, the role of mechanical forces in the collective behavior of bacterial colonies is not yet fully understood. Here, we construct a model of growing rod-like bacteria, such as Escherichia coli based purely on mechanical forces. We perform overdamped molecular dynamics simulations of the colony starting from a few cells in contact with a surface. As the colony grows, microdomains of strongly aligned cells grow and proliferate. Our model captures both the initial growth of a bacterial colony and also shows characteristic signs of capturing the experimentally observed transition to multilayered colonies over longer timescales. We compare our results with experiments on E. coli cells and analyze the statistics of microdomains.

References

Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M., Annu. Rev. Microbiol., 1995, 49, No. 1, 711–745, https://doi.org/10.1146/annurev.mi.49.100195.003431. DOI: https://doi.org/10.1146/annurev.mi.49.100195.003431

Hartmann R., Singh P. K., Pearce P., Mok R., Song B., Díaz-Pascual F., Dunkel J., Drescher K., Nat. Phys., 2019, 15, No. 3, 251–256, https://doi.org/10.1038/s41567-018-0356-9. DOI: https://doi.org/10.1038/s41567-018-0356-9

Flemming H.-C., Wingender J., Nat. Rev. Microbiol., 2010, 8, No. 9, 623–633, https://doi.org/10.1038/nrmicro2415. DOI: https://doi.org/10.1038/nrmicro2415

Araújo N. A. M., Janssen L. M. C., Barois T., Boffetta G., Cohen I., Corbetta A., Dauchot O., Dijkstra M., Durham W. M., Dussutour A., et al., Soft Matter, 2023, 19, 1695–1704, https://doi.org/10.1039/D2SM01562E. DOI: https://doi.org/10.1039/D2SM01562E

Nijjer J., Li C., Zhang Q., Lu H., Zhang S., Yan J., Nat. Commun., 2021, 12, No. 1, 6632, https://doi.org/10.1038/s41467-021-26869-6. DOI: https://doi.org/10.1038/s41467-021-26869-6

Sengupta A., Front. Phys., 2020, 8, No. 184, https://doi.org/10.3389/fphy.2020.00184. DOI: https://doi.org/10.3389/fphy.2020.00184

Allen R. J., Waclaw B., Rep. Prog. Phys., 2018, 82, No. 1, 016601, https://doi.org/10.1088/1361-6633/aae546. DOI: https://doi.org/10.1088/1361-6633/aae546

Drescher K., Dunkel J., Nadell C. D., Van Teeffelen S., Grnja I., Wingreen N. S., Stone H. A., Bassler B. L., PNAS, 2016, 113, No. 14, E2066–E2072, https://doi.org/10.1073/pnas.1601702113. DOI: https://doi.org/10.1073/pnas.1601702113

Karimi A., Karig D., Kumar A., Ardekani A. M., Lab Chip, 2015, 15, No. 1, 23–42, https://doi.org/10.1039/C4LC01095G. DOI: https://doi.org/10.1039/C4LC01095G

Farrell F. D. C., Hallatschek O., Marenduzzo D., Waclaw B., Phys. Rev. Lett., 2013, 111, No. 16, 168101, https://doi.org/10.1103/PhysRevLett.111.168101. DOI: https://doi.org/10.1103/PhysRevLett.111.168101

Tiron R., Mallon F., Dias F., Reynaud E. G., Renewable Sustainable Energy Rev., 2015, 43, 1263–1272, https://doi.org/10.1016/j.rser.2014.11.105. DOI: https://doi.org/10.1016/j.rser.2014.11.105

Hall-Stoodley L., Costerton J. W., Stoodley P., Nat. Rev. Microbiol., 2004, 2, No. 2, 95–108, https://doi.org/10.1038/nrmicro821. DOI: https://doi.org/10.1038/nrmicro821

Mazza M. G., J. Phys. D: Appl. Phys., 2016, 49, No. 20, 203001, https://doi.org/10.1088/0022-3727/49/20/203001. DOI: https://doi.org/10.1088/0022-3727/49/20/203001

You Z., Pearce D. J., Sengupta A., Giomi L., Phys. Rev. X, 2018, 8, No. 3, 031065, https://doi.org/10.1103/PhysRevX.8.031065. DOI: https://doi.org/10.1103/PhysRevX.8.031065

You Z., Pearce D. J., Sengupta A., Giomi L., Phys. Rev. Lett., 2019, 123, No. 17, 178001, https://doi.org/10.1103/PhysRevLett.123.178001. DOI: https://doi.org/10.1103/PhysRevLett.123.178001

Dell’Arciprete D., Blow M. L., Brown A. T., Farrell F. D. C., Lintuvuori J. S., McVey A. F., Marenduzzo D., Poon W. C. K., Nat. Commun., 2018, 9, No. 1, 4190, https://doi.org/10.1038/s41467-018-06370-3. DOI: https://doi.org/10.1038/s41467-018-06370-3

Boyer D., Mather W., Mondragón-Palomino O., Orozco-Fuentes S., Danino T., Hasty J., Tsimring L. S., Phys. Biol., 2011, 8, No. 2, 026008, https://doi.org/10.1088/1478-3975/8/2/026008. DOI: https://doi.org/10.1088/1478-3975/8/2/026008

Sheats J., Sclavi B., Cosentino Lagomarsino M., Cicuta P., Dorfman K. D., R. Soc. Open Sci., 2017, 4, No. 6, 170463, https://doi.org/10.1098/rsos.170463. DOI: https://doi.org/10.1098/rsos.170463

Beroz F., Yan J., Meir Y., Sabass B., Stone H. A., Bassler B. L., Wingreen N. S., Nat. Phys., 2018, 14, No. 9, 954–960, https://doi.org/10.1038/s41567-018-0170-4. DOI: https://doi.org/10.1038/s41567-018-0170-4

Dhar J., Thai A. L. P., Ghoshal A., Giomi L., Sengupta A., Nat. Phys., 2022, 18, No. 8, 945–951, https://doi.org/10.1038/s41567-022-01641-9. DOI: https://doi.org/10.1038/s41567-022-01641-9

Earl D. J., Ilnytskyi J., Wilson M. R., Mol. Phys., 2001, 99, No. 20, 1719–1726, https://doi.org/10.1080/00268970110069551. DOI: https://doi.org/10.1080/00268970110069551

Pearce P., Song B., Skinner D. J., Mok R., Hartmann R., Singh P. K., Jeckel H., Oishi J. S., Drescher K., Dunkel J., Phys. Rev. Lett., 2019, 123, No. 25, 258101, https://doi.org/10.1103/PhysRevLett.123.258101. DOI: https://doi.org/10.1103/PhysRevLett.123.258101

Volfson D., Cookson S., Hasty J., Tsimring L. S., PNAS, 2008, 105, No. 40, 15346–15351, https://doi.org/10.1073/pnas.0706805105. DOI: https://doi.org/10.1073/pnas.0706805105

Vega C., Lago S., Comput. Chem., 1994, 18, No. 1, 55–59, https://doi.org/10.1016/0097-8485(94)80023-5. DOI: https://doi.org/10.1016/0097-8485(94)80023-5

Wittmann R., Nguyen G. P., Löwen H., Schwarzendahl F. J., Sengupta A., Commun. Phys., 2023, 6, No. 1, 331, https://doi.org/10.1038/s42005-023-01449-w. DOI: https://doi.org/10.1038/s42005-023-01449-w

Willis L., Huang K. C., Nat. Rev. Microbiol., 2017, 15, No. 10, 606–620, https://doi.org/10.1038/nrmicro.2017.79. DOI: https://doi.org/10.1038/nrmicro.2017.79

Jun S., Si F., Pugatch R., Scott M., Rep. Prog. Phys., 2018, 81, No. 5, 056601, https://doi.org/10.1088/1361-6633/aaa628. DOI: https://doi.org/10.1088/1361-6633/aaa628

Su P.-T., Liao C.-T., Roan J.-R., Wang S.-H., Chiou A., Syu W.-J., PloS ONE, 2012, 7, No. 11, e48098, https://doi.org/10.1371/journal.pone.0048098. DOI: https://doi.org/10.1371/journal.pone.0048098

Grant M. A. A., Wacław B., Allen R. J., Cicuta P., J. R. Soc. Interface, 2014, 11, No. 97, 20140400, https://doi.org/10.1098/rsif.2014.0400. DOI: https://doi.org/10.1098/rsif.2014.0400

Ilnytskyi J. M., Trokhymchuk A., Schoen M., J. Chem. Phys., 2014, 141,No. 11, 114903, https://doi.org/10.1063/1.4894438. DOI: https://doi.org/10.1063/1.4894438

Ester M., Kriegel H.-P., Sander J., Xu X., In: Proceedings of the Second International Conference on Knowledge Discovery and Data Mining (KDD-96), AAAI, 1996, 226–231.

Paget J., Mazza M. G., Archer A. J., Shendruk T. N., Nat. Commun., 2023, 14, No. 1, 1048, https://doi.org/10.1038/s41467-023-36506-z. DOI: https://doi.org/10.1038/s41467-023-36506-z

Paget J., Alberti U., Mazza M. G., Archer A. J., Shendruk T. N., J. Phys. A: Math. Theor., 2022, 55, No. 35, 354001, https://doi.org/10.1088/1751-8121/ac80df. DOI: https://doi.org/10.1088/1751-8121/ac80df

Published

2024-03-28

How to Cite

[1]
M. T. Khan, J. Cammann, A. Sengupta, E. Renzi, and M. G. Mazza, “Toward a realistic model of multilayered bacterial colonies”, Condens. Matter Phys., vol. 27, no. 1, p. 13802, Mar. 2024, doi: 10.5488/cmp.27.13802.