Systematic Perturbation of Cytoskeletal Function Reveals a Linear Scaling Relationship between Cell Geometry and Fitness

• Published in: Cell reports (Cambridge) Vol. 9; no. 4; pp. 1528 - 1537
• Main Authors: Monds, Russell D., Lee, Timothy K., Colavin, Alexandre, Ursell, Tristan, Quan, Selwyn, Cooper, Tim F., Huang, Kerwyn Casey
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 20.11.2014; Elsevier
• Subjects: Alleles; Clone Cells; Cytoskeleton - metabolism; Directed Molecular Evolution; Environment; Escherichia coli - cytology; Escherichia coli - genetics; Escherichia coli - metabolism; Escherichia coli Proteins - metabolism; Genetic Fitness; Mutation
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2014.10.040

Diversification of cell size is hypothesized to have occurred through a process of evolutionary optimization, but direct demonstrations of causal relationships between cell geometry and fitness are lacking. Here, we identify a mutation from a laboratory-evolved bacterium that dramatically increases cell size through cytoskeletal perturbation and confers a large fitness advantage. We engineer a library of cytoskeletal mutants of different sizes and show that fitness scales linearly with respect to cell size over a wide physiological range. Quantification of the growth rates of single cells during the exit from stationary phase reveals that transitions between “feast-or-famine” growth regimes are a key determinant of cell-size-dependent fitness effects. We also uncover environments that suppress the fitness advantage of larger cells, indicating that cell-size-dependent fitness effects are subject to both biophysical and metabolic constraints. Together, our results highlight laboratory-based evolution as a powerful framework for studying the quantitative relationships between morphology and fitness. [Display omitted] •Genetic tools for fine-scale control of cell geometry are developed•Bacterial fitness scales linearly as a function of cell size over a wide range•Transitions between “feast-or-famine” regimes underlie size-dependent fitness effects•Cell-size fitness effects are subject to biophysical and metabolic constraints Monds et al. isolate a mutation from a laboratory-evolved bacterium that dramatically increases cell size through cytoskeletal perturbation and confers a large fitness advantage. They engineer a library of cytoskeletal mutants of different sizes and demonstrate that fitness scales linearly with cell size through accelerated transitions between “feast-or-famine” growth regimes.