Flagellar dynamics reveal fluctuations and kinetic limit in the Escherichia coli chemotaxis network

• Published in: Scientific reports Vol. 13; no. 1; pp. 22891 - 16
• Main Authors: Bano, Roshni, Mears, Patrick, Golding, Ido, Chemla, Yann R.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 21.12.2023; Nature Publishing Group; Nature Portfolio
• Subjects: 631/553; 631/553/2707; 631/57; 631/57/343; 631/57/343/1361; Chemotaxis; CheY protein; E coli; Escherichia coli; Flagella; Fluctuations; Fluorescence microscopy; Gene expression; Humanities and Social Sciences; multidisciplinary; Science; Science (multidisciplinary); Swimming; Tumbling
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-023-49784-w

The Escherichia coli chemotaxis network, by which bacteria modulate their random run/tumble swimming pattern to navigate their environment, must cope with unavoidable number fluctuations (“noise”) in its molecular constituents like other signaling networks. The probability of clockwise (CW) flagellar rotation, or CW bias, is a measure of the chemotaxis network’s output, and its temporal fluctuations provide a proxy for network noise. Here we quantify fluctuations in the chemotaxis signaling network from the switching statistics of flagella, observed using time-resolved fluorescence microscopy of individual optically trapped E. coli cells. This approach allows noise to be quantified across the dynamic range of the network. Large CW bias fluctuations are revealed at steady state, which may play a critical role in driving flagellar switching and cell tumbling. When the network is stimulated chemically to higher activity, fluctuations dramatically decrease. A stochastic theoretical model, inspired by work on gene expression noise, points to CheY activation occurring in bursts, driving CW bias fluctuations. This model also shows that an intrinsic kinetic ceiling on network activity places an upper limit on activated CheY and CW bias, which when encountered suppresses network fluctuations. This limit may also prevent cells from tumbling unproductively in steep gradients.