Origin of temperature dependence of bacterial growth rate: Analogy with the viscosity of glass-forming liquids in inorganic materials

Authors

DOI:

https://doi.org/10.33910/2687-153X-2024-5-2-67-73

Keywords:

bacterial growth rate, glass-forming liquid, glass transition, viscosity, free volume

Abstract

Based on a recent suggestion that the bacterial cytoplasm has a property similar to glass-forming liquids, we have proposed a new relation for the temperature dependence of the bacterial growth rate, k = k0exp[–Ea/kB(TTc)] in the lower temperature range, where k0 is a constant, Ea is the activation energy (eV), kB is the Boltzmann constant, T is the absolute temperature (K), and Tc is the characteristic (frozen-in) temperature (K), resembling the temperature-dependent fluidity (inverse viscosity) observed in glass-forming liquids in inorganic materials. This monotonic behavior of bacterial growth breaks down at higher temperatures, that is, k decreases rapidly with T. This may be attributed to a rapid increase in the physiological cytoplasmic concentration above the critical temperature Tm. The finding on the temperaturedependent bacterial growth rate is analogous to that observed in glass-forming liquids in non-living inorganic materials.

References

Arcus, V. L., Prentice, E. J., Hobbs, J. K. et al. (2016) On the temperature dependence of enzyme-catalyze rates. Biochemistry, 55 (12), 1681–1688. https://doi.org/10.1021/acs.biochem.5b01094 (In English)

Balasubramanian, S., Devi, A., Singh, K. et al. (2016) Application of glass transition in food processing. Critical Reviews in Food Science and Nutrition, 56 (6), 919–936. https://doi.org/10.1080/10408398.2012.734343 (In English)

Berthier, L., Flenner, E., Szamel, G. (2019) Glassy dynamics in dense systems of active particles. The Journal of Chemical Physics, 150 (20), article 200901. https://doi.org/https://doi.org/10.1063/1.5093240 (In English)

Cossins, B., Jacobson, M. P., Guallar, V. (2011) A new view of the bacterial cytosol environment. PLOS Computer Biology, 7 (6), article e1002066. https://doi.org/10.1371/journal.pcbi.1002066 (In English)

Dauchot, O., Lowen, H. (2019) Chemical physics of active matter. The Journal of Chemical Physics, 151 (11), article 114901. https://doi.org/10.1063/1.5125902 (In English)

Fernandez-de-Cossio-Diaz, J. F., Vazquez, A. (2018) A physical model of cell metabolism. Scientific Reports, 8 (1), article 8349. https://doi.org/10.1038/s41598-018-26724-7 (In English)

Doolittle, A. K. (1951) Studies in Newtonian Flow. II. The dependence of the viscosity of liquids on free-space. Journal of Applied Physics, 22 (12), 1471–1475. https://doi.org/10.1063/1.1699894 (In English)

Elliott, S. R. (1990) Physics of amorphous materials. 2nd ed. New York: Wiley Publ., 481 p. (In English)

Golding, I., Cox, E. C. (2006) Physical nature of bacterial cytoplasm. Physical Review Letters, 96 (9), article 098102. https://doi.org/10.1103/PhysRevLett.96.098102 (In English)

Grimaldo, M., Lopez, H., Beck, C. et al. (2019) Protein short-time diffusion in a naturally crowded environment. The Journal of Physical Chemistry Letters, 10 (8), 1709−1715. https://doi.org/10.1021/acs.jpclett.9b00345 (In English)

Heitezer, H., Peter, H., Kohler, E., Hamer, G. (1991) Utility of phenomenological models for describing temperature dependence of bacterial growth. Applied and Environmental Biology, 57 (9), 2656−2665. https://doi.org/10.1128/aem.57.9.2656-2665.1991 (In English)

Janssen, L. M. C. (2019) Active glasses. Journal of Physics: Condensed Matter, 31, article 503002. https://doi.org/10.1088/1361-648X/ab3e90 (In English)

Khonsari, A. S., Kollmann, M. (2015) Perception and regulatory principles of microbial growth control. PLoS ONE, 10 (5), article e0126244. https://doi.org/10.1371/journal.pone.0126244 (In English)

Lama, H., Yamamoto, M. J., Furuta, Y. et al. (2022) Emergence of bacterial glass. [Online]. Available at: https://arxiv.org/abs/2205.10436 (accessed 09.11.2023). (In English)

Lee, K., Shoda, M., Kawai, K., Koseki, S. (2020) Relationship between glass transition temperature, and desiccation and heat tolerance in Salmonella enterica. PLoS ONE, 15 (5), article e0233638. https://doi.org/10.1371%2Fjournal.pone.0233638 (In English)

Micoulaut, M. (2021) The world scientific reference of amorphous materials: Structure, properties, modeling and applications of amorphous chalcogenides. New Jersey: World Scientific Publ., 1548 p. (In English)

Munder, M. C., Midtvedt, D., Franzmann, T. et al. (2016) A pH-driven transition of the cytoplasm from a fluid-to a solid-like state promotes entry into dormancy. eLife, 5, article e09347. https://doi.org/10.7554/eLife.09347 (In English)

Nishizawa, K., Fujiwara, K., Ikenaga, M., Nakajo, N. (2017) Universal glass-forming behavior of in vitro and living cytoplasm. Scientific Report, 7 (1), article 15143. https://doi.org/10.1038/s41598-017-14883-y (In English)

Noll, P., Lilge, L, Hausmann, R., Henkel, M. (2020) Modeling and exploiting microbial temperature response. Processes, 8 (1), article 121. https://doi.org/10.3390/pr8010121 (In English)

Ojovan, M. I. (2008) Viscosity and glass transition in amorphous oxides. Advanced in Condensed Physics, 2008, article 817829. https://doi.org/10.1155/2008/817829 (In English)

Oyama, N., Kawasaki, T., Mizuno, K., Ikeda, A. (2019) Glassy dynamics of a model of bacterial cytoplasm with metabolic activities. Physical Review Research, 1 (3), article 032038(R). https://doi.org/10.1103/PhysRevResearch.1.032038 (In English)

Perry, B. R., Surovtsev, I. V., Cabeen, M. T. et al. (2014) The bacterial cytoplasm has glass-like properties and is fluidized by metabolic activity. Cell, 156 (1–2), 183–194. https://doi.org/10.1016/j.cell.2013.11.028 (In English)

Pinto, C., Shimakawa, K. (2023) Glassy dynamics in bacterial growth rate temperature dependence. AIP Advances, 13 (2), article 025126. https://doi.org/10.1063/5.0139055 (In English)

Ratkowsky, D. A., Lowry, R. K., McMeekin, T. A. et al. (1983) Model for bacterial culture growth rate throughout the entire biokinetic temperature range. Journal of Bacteriology, 154 (3), 1222–1226. https://doi.org/10.1128/jb.154.3.1222-1226.1983 (In English)

Ratkowsky, D. A., Olley, J., McMeekin, T. A., Ball, A. (1982) Relationship between temperature and growth rate of bacterial cultures. Journal of Bacteriology, 149 (1), 1–5. https://doi.org/10.1128/jb.149.1.1-5.1982 (In English)

Ryabov, Ya. E., Gutina, A., Arkhipov, V., Feldman, Yu. (2001) Dielectric relaxation of water absorbed in porous glass. The Journal of Physical Chemistry B, 105 (9), 1845–1850. https://doi.org/10.1021/jp0033061 (In English)

Ryabov, Ya. E., Puzenko, A., Feldman, Yu. (2004) Nonmonotonic relaxation kinetics of confined systems. Physical Review B, 69 (1), article 014204. https://doi.org/10.1103/PhysRevB.69.014204 (In English)

Smigiel, W. M., Mantovanelli, L., Linnik, D. et al. (2022) Protein diffusion in Escherichia coli cytoplasm scales with the mass of the complexes and is location dependent. Science Advances, 8 (32), article eabo5387. https://doi.org/10.1126/sciadv.abo5387 (In English)

Takatori, S. C., Mandadapu, K. K. (2020) Motility-induced buckling and glassy dynamics regulate 3D transitions of bacterial monolayers. [Online]. Available at: https://arxiv.org/abs/2003.05618 (accessed 12.03.2024). (In English)

Tanaka, K., Shimakawa, K. (2021) Amorphous Chalcogenide Semiconductors and Related Materials. New York: Springer Publ., 300 p. (In English)

Trevors, J. T., van Elsas, D. J., Bej, A. K. (2013) The molecularly crowded cytoplasm of bacterial cells: Dividing cells contrasted with viable but non-culturable (VBNC) bacterial cells. Current Issues in Molecular Biology, 15, 1–6. https://doi.org/10.21775/cimb.015.001 (In English)

Yu, I., Mori, T., Ando, T. et al. (2016) Biomolecular interactions modulate macromolecular structure and dynamics in atomistic model of a bacterial cytoplasm. eLife, 5 (1), article 19274. https://doi.org/10.7554/eLife.19274 (In English)

Zallen, R. (1983) The physics of amorphous solids. New York: John Wiley and Sons Publ., 304 p. (In English)

Published

24.06.2024

Issue

Section

Condensed Matter Physics