A bacterial size law revealed by a coarse-grained model of cell physiology

AbstractUniversal observations in Biology are sometimes described as “laws”. InE. coli, experimental studies performed over the past six decades have revealed major growth laws relating ribosomal mass fraction and cell size to the growth rate. Because they formalize complex emerging principles in biology, growth laws have been instrumental in shaping our understanding of bacterial physiology. Here, we discovered a novel size law that connects cell size to the inverse of the metabolic proteome mass fraction and the active fraction of ribosomes. We used a simple whole-cell coarse-grained model of cell physiology that combines the proteome allocation theory and the structural model of cell division. The model captures all available experimental data connecting the cell proteome composition, ribosome activity, division size and growth rate in response to nutrient quality, antibiotic treatment and increased protein burden. Finally, a stochastic extension of the model explains non-trivial correlations observed in single cell experiments including the adder principle. This work provides a simple and robust theoretical framework for studying the fundamental principles of cell size determination in unicellular organisms.

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Quantitative insights into the cyanobacterial cell economy

eLife ◽

10.7554/elife.42508 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 20

Author(s):

Tomáš Zavřel ◽

Marjan Faizi ◽

Cristina Loureiro ◽

Gereon Poschmann ◽

Kai Stühler ◽

...

Keyword(s):

Growth Rate ◽

Coarse Grained ◽

Translational Machinery ◽

Coarse Grained Model ◽

Green Biotechnology ◽

Photosynthetic Productivity ◽

Heterotrophic Microorganisms ◽

Wide Range ◽

Growth Laws ◽

Phototrophic Growth

Phototrophic microorganisms are promising resources for green biotechnology. Compared to heterotrophic microorganisms, however, the cellular economy of phototrophic growth is still insufficiently understood. We provide a quantitative analysis of light-limited, light-saturated, and light-inhibited growth of the cyanobacterium Synechocystis sp. PCC 6803 using a reproducible cultivation setup. We report key physiological parameters, including growth rate, cell size, and photosynthetic activity over a wide range of light intensities. Intracellular proteins were quantified to monitor proteome allocation as a function of growth rate. Among other physiological acclimations, we identify an upregulation of the translational machinery and downregulation of light harvesting components with increasing light intensity and growth rate. The resulting growth laws are discussed in the context of a coarse-grained model of phototrophic growth and available data obtained by a comprehensive literature search. Our insights into quantitative aspects of cyanobacterial acclimations to different growth rates have implications to understand and optimize photosynthetic productivity.

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Optimal proteome allocation and the temperature dependence of microbial growth laws

npj Systems Biology and Applications ◽

10.1038/s41540-021-00172-y ◽

2021 ◽

Vol 7 (1) ◽

Author(s):

Francis Mairet ◽

Jean-Luc Gouzé ◽

Hidde de Jong

Keyword(s):

Growth Rate ◽

Stress Responses ◽

Protein Unfolding ◽

Microbial Growth ◽

Coarse Grained ◽

Effect Of Temperature ◽

Temperature Sensitive ◽

Coarse Grained Model ◽

Proteomic Data ◽

Growth Laws

AbstractAlthough the effect of temperature on microbial growth has been widely studied, the role of proteome allocation in bringing about temperature-induced changes remains elusive. To tackle this problem, we propose a coarse-grained model of microbial growth, including the processes of temperature-sensitive protein unfolding and chaperone-assisted (re)folding. We determine the proteome sector allocation that maximizes balanced growth rate as a function of nutrient limitation and temperature. Calibrated with quantitative proteomic data for Escherichia coli, the model allows us to clarify general principles of temperature-dependent proteome allocation and formulate generalized growth laws. The same activation energy for metabolic enzymes and ribosomes leads to an Arrhenius increase in growth rate at constant proteome composition over a large range of temperatures, whereas at extreme temperatures resources are diverted away from growth to chaperone-mediated stress responses. Our approach points at risks and possible remedies for the use of ribosome content to characterize complex ecosystems with temperature variation.

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Quantitative insights into the cyanobacterial cell economy

10.1101/446179 ◽

2018 ◽

Cited By ~ 1

Author(s):

Tomáš Zavřel ◽

Marjan Faizi ◽

Cristina Loureiro ◽

Gereon Poschmann ◽

Kai Stühler ◽

...

Keyword(s):

Growth Rate ◽

Coarse Grained ◽

Translational Machinery ◽

Coarse Grained Model ◽

Green Biotechnology ◽

Photosynthetic Productivity ◽

Heterotrophic Microorganisms ◽

Wide Range ◽

Growth Laws ◽

Phototrophic Growth

AbstractPhototrophic microorganisms are promising resources for green biotechnology. Compared to heterotrophic microorganisms, however, the cellular economy of phototrophic growth is still insufficiently understood. We provide a quantitative analysis of light-limited, light-saturated, and light-inhibited growth of the cyanobacteriumSynechocystissp. PCC 6803 using a reproducible cultivation setup. We report key physiological parameters, including growth rate, cell size, and photosynthetic activity over a wide range of light intensities. Intracellular proteins were quantified to monitor proteome allocation as a function of growth rate. Among other physiological adaptations, we identify an upregulation of the translational machinery and downregulation of light harvesting components with increasing light intensity and growth rate. The resulting growth laws are discussed in the context of a coarse-grained model of phototrophic growth and available data obtained by a comprehensive literature search. Our insights into quantitative aspects of cyanobacterial adaptations to different growth rates have implications to understand and optimize photosynthetic productivity.

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Resource allocation to cell envelopes and the scaling of bacterial growth rate

10.1101/2022.01.07.475415 ◽

2022 ◽

Author(s):

Bogi Trickovic ◽

Michael Lynch

Keyword(s):

Growth Rate ◽

Mass Fraction ◽

Cell Envelope ◽

Empirical Studies ◽

Volume Ratio ◽

Coarse Grained ◽

Proteomics Data ◽

Bacterial Growth Rate ◽

Bacterial Physiology ◽

Cell Envelopes

Although various empirical studies have reported a positive correlation between the specific growth rate and cell size across bacteria, it is currently unclear what causes this relationship. We conjecture that such scaling occurs because smaller cells have a larger surface-to-volume ratio and thus have to allocate a greater fraction of the total resources to the production of the cell envelope, leaving fewer resources for other biosynthetic processes. To test this theory, we developed a coarse-grained model of bacterial physiology composed of the proteome that converts nutrients into biomass, with the cell envelope acting as a resource sink. Assuming resources are partitioned to maximize the growth rate, the model yields expected scalings. Namely, the growth rate and ribosomal mass fraction scale negatively, while the mass fraction of envelope-producing enzymes scales positively with surface-to-volume. These relationships are compatible with growth measurements and quantitative proteomics data reported in the literature.

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