PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

Abstract

Chemoreceptors provide sensory specificity and sensitivity that enable motile bacteria to seek optimal positions for growth and metabolism in gradients of various physicochemical cues. Despite the abundance of chemoreceptors, little is known regarding the sensory specificity and the exact contribution of individual chemoreceptors to the lifestyle of bacteria. Azospirillum brasilense are motile bacteria that can fix atmospheric nitrogen under microaerophilic conditions. Here, we characterized a chemoreceptor in this organism, named AerC, which functions as a redox sensor that enables the cells to seek microaerophilic conditions that support optimum nitrogen fixation. AerC is a representative of a widespread class of soluble chemoreceptors that monitor changes in the redox status of the electron transport system via the FAD cofactor associated with its PAS domains. In A. brasilense, AerC clusters at the cell poles. Its cellular localization and contribution to the behavioral response correlate with its expression pattern and with changes in the overall cellular FAD content under nitrogenfixing conditions. AerC-mediated energy taxis in A. brasilense prevails under conditions of nitrogen fixation, illustrating a strategy by which cells optimize chemosensing to signaling cues that directly affect current metabolic activities and thus revealing a mechanism by which chemotaxis is coordinated with dynamic changes in cell physiology.FAD | nitrogen fixation | signal transduction M otile bacteria detect changes in environmental conditions and respond by navigating toward niches where conditions are optimal for growth. This widespread behavior is collectively known as chemotaxis (1). Various physicochemical cues are detected by dedicated chemoreceptors (methyl-accepted chemotaxis proteins or MCPs) that relay information to the flagellar motors via a signal transduction cascade (2). The model organism for chemotaxis, Escherichia coli, possesses five transmembrane chemoreceptors (Tar, Tsr, Tap, Trg, and Aer) and the sensory specificities for each of these have been determined (2). Most bacterial species have a greater number of chemoreceptors than E. coli (3); however, their sensory specificities and contribution to the lifestyle of bacteria are virtually unknown.Azospirillum brasilense are motile bacteria that can fix atmospheric nitrogen under microaerophilic conditions. These bacteria respond tactically to various chemoeffectors that affect their metabolism and the resulting changes in energy levels function as signals (4). In oxygen gradients, A. brasilense cells quickly navigate to a specific zone where oxygen concentration is low enough (3-5 μM) to support their microaerobic lifestyle and to be compatible with nitrogen fixation (5). Chemotactic responses to changes in energy metabolism have been identified in several bacterial species and are collectively referred to as "energy taxis" (6). In E. coli, two of the five chemoreceptors have been implicated in mediating energy taxis: Aer, which senses the redox status via an...

Internal Sense of Direction: Sensing and Signaling from Cytoplasmic Chemoreceptors

“…A. brasilense codes for four chemotaxis pathways, with 51 chemoreceptors. AerC AB is a cytoplasmic chemoreceptor that possesses two N-terminal PAS domains and a C-terminal MA domain (12). AerC AB binds FAD at each of two N-terminal PAS domains and is postulated to sense intracellular redox, via the bound FAD, and direct an oxygen-repellent response to support nitrogen fixation (12).…”

“…In all cytoplasmic chemoreceptors, the PAS domain was located N terminal to the MA domain (Table 1). A few PAS-containing cytoplasmic chemoreceptors have been implicated in energy taxis, a motility-based response for positioning cells in an optimum microenvironment for energy generation (12,15) (Table 1).…”

“…AerC AB is a cytoplasmic chemoreceptor that possesses two N-terminal PAS domains and a C-terminal MA domain (12). AerC AB binds FAD at each of two N-terminal PAS domains and is postulated to sense intracellular redox, via the bound FAD, and direct an oxygen-repellent response to support nitrogen fixation (12). AerC AB -YFP localization was determined by fluorescence microscopy and was found to be both diffuse in the cytoplasm and localized in foci at the pole, depending on growth conditions (Fig.…”

“…Furthermore, chemoreceptors can function in processes other than motility, e.g., gene regulation (8). Cytoplasmic chemoreceptors, however, are known to play important roles in many microbial processes, including pathogenesis (9,10), fruiting body formation (8), as well as mediating taxis in response to cellular energy stores (11,12), redox (13,14), and metabolites (15). In this review, we first start with a discussion of basic chemoreceptor attributes and then summarize the current state of understanding about signal recognition, signal transduction, and the subcellular localization of cytoplasmic chemoreceptors.…”

Metabolism Dependent Chemotaxis of Pseudomonas aeruginosa N1 Towards Anionic Detergent Sodium Dodecyl Sulfate

“…An increase or decrease in energy level is perceived as a signal [30]. Molecules that take part in this process are terminal electron acceptors, light, redox-active compounds and metabolizable substrates that are electron donors [31]. The best example of this kind of receptor system is exhibited by Aer protein of E. coli, which is responsible for aerotaxis.…”