Abstract
Bacteria move towards favourable and away from toxic environments by changing their swimming pattern. This response is regulated by the chemotaxis signalling pathway, which has an important feature: it uses feedback to ‘reset’ (adapt) the bacterial sensing ability, which allows the bacteria to sense a range of background environmental changes. The role of this feedback has been studied extensively in the simple chemotaxis pathway of Escherichia coli. However it has been recently found that the majority of bacteria have multiple chemotaxis homologues of the E. coli proteins, resulting in more complex pathways. In this paper we investigate the configuration and role of feedback in Rhodobacter sphaeroides, a bacterium containing multiple homologues of the chemotaxis proteins found in E. coli. Multiple proteins could produce different possible feedback configurations, each having different chemotactic performance qualities and levels of robustness to variations and uncertainties in biological parameters and to intracellular noise. We develop four models corresponding to different feedback configurations. Using a series of carefully designed experiments we discriminate between these models and invalidate three of them. When these models are examined in terms of robustness to noise and parametric uncertainties, we find that the non-invalidated model is superior to the others. Moreover, it has a ‘cascade control’ feedback architecture which is used extensively in engineering to improve system performance, including robustness. Given that the majority of bacteria are known to have multiple chemotaxis pathways, in this paper we show that some feedback architectures allow them to have better performance than others. In particular, cascade control may be an important feature in achieving robust functionality in more complex signalling pathways and in improving their performance.
Highlights
Living organisms respond to changes in their internal and external environment in order to survive
Bacteria move towards favourable environments by changing their swimming pattern
An important feature of this response, which is called bacterial chemotaxis, is that their sensing ability remains independent of the background environment in which they find themselves
Summary
Living organisms respond to changes in their internal and external environment in order to survive. The sensing, signalling and response mechanisms often consist of complicated pathways the dynamical behaviour of which is often difficult to understand without mathematical models [1]. Considering the structure and dynamics of these signalling pathways as integrated dynamical systems can help us understand how the pathway architecture and parameter values result in the performance and robustness in the response dynamics [2]. One extensively studied sensory pathway is bacterial chemotaxis. This pathway controls changes in bacterial motion in response to environmental stimuli, biasing movement towards regions of higher concentration of beneficial or lower concentration of toxic chemicals. The chemotaxis signalling pathway in the bacterium Escherichia coli is a simple network with one feedback loop [3] which has been extensively studied and used as a paradigm for the mechanism of chemotaxis signalling networks [4]. In E. coli, chemical ligands bind to methyl-accepting chemotaxis protein (MCP) receptors that span the cell membrane and alter the activity of a cytoplasmic histidine kinase called CheA
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