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.2024 Oct 8;121(41):e2412541121.
doi: 10.1073/pnas.2412541121. Epub 2024 Oct 1.

Flagellar motility is mutagenic

Affiliations

Flagellar motility is mutagenic

Souvik Bhattacharyya et al. Proc Natl Acad Sci U S A..

Abstract

Flagella are highly complex rotary molecular machines that enable bacteria to not only migrate to optimal environments but also to promote range expansion, competitiveness, virulence, and antibiotic survival. Flagellar motility is an energy-demanding process, where the sum of its production (biosynthesis) and operation (rotation) costs has been estimated to total ~10% of the entire energy budget of anEscherichia coli cell. The acquisition of such a costly adaptation process is expected to secure short-term benefits by increasing competitiveness and survival, as well as long-term evolutionary fitness gains. While the role of flagellar motility in bacterial survival has been widely reported, its direct influence on the rate of evolution remains unclear. We show here that both production and operation costs contribute to elevated mutation rates. Our findings suggest that flagellar movement may be an important player in tuning the rate of bacterial evolution.

Keywords: E. coli; evolution; flagella; mutation.

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Conflict of interest statement

Competing interests statement:The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Flagellar motility and mutation rate are positively correlated. (A) Flagella and chemotaxis components (SI Appendix). Mutated genes are labeled in red. (B) Operational and production costs of deletion (Δ) and overexpression (↑) strains. (C) Swimming motility (6 h) of various strains assayed on soft agar (n = 6); v, empty vector control. (D) Mutation rate per genome (µg) of indicated strains measured as Rif50-resistant colony forming units (CFUs) per unit CFU (n = 9). The ±fold-change in µg (in parenthesis) compared to WT is as follows: ΔmotA (−3.6); ΔfliC (−3); ΔmotAΔfliC (−9.2); ΔflhDC (−10.5);fliT↑ (−3); andflhDC↑ (+3.8).P values from Mann–Whitney;∗∗∗P < 0.001,∗∗∗∗P < 0.0001.
Fig. 2.
Fig. 2.
Mutagenicity of flagellar motility is ROS derived. (A) ROS levels in different strains (n = 6);P values from Mann–Whitney. (B) Brightfield (BF) and ROS fluorescence images. (C) Cellular respiration was estimated by CTC staining (n = 6);P values from Wilcoxon rank-sum. (D) µg; ±GSH, 50 mM glutathione. (Right) Restoration of µg after complementation;P values from Wilcoxon rank sum (Left) or Mann–Whitney (Right);∗∗∗P < 0.001,∗∗∗∗P < 0.0001. (E) Correlation of µg and flagellar energy cost of all strains (except WT/fliT↑) using data in Fig. 1B andD, respectively; RSpearman = 0.9212.
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References

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