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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 nitrogen-fixing 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.

SUBMITTER: Xie Z

PROVIDER: S-EPMC2836669 | biostudies-literature | 2010 Feb

REPOSITORIES: biostudies-literature

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PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis.

Xie Zhihong Z Ulrich Luke E LE Zhulin Igor B IB Alexandre Gladys G

Proceedings of the National Academy of Sciences of the United States of America 20100119 5

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 c ...[more]

PMID: 20133866

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Project description:Chemotaxis is an important virulence factor in some enteric pathogens, and it is involved in the pathogenesis and colonization of the host. However, there is limited knowledge regarding the environmental signals that promote chemotactic behavior and the sensing of these signals by chemoreceptors. To date, there is no information on the ligand molecule that directly binds to and is sensed by Campylobacter jejuni Tlp1, which is a chemoreceptor with a dCache-type ligand-binding domain (LBD). dCache (double Calcium channels and chemotaxis receptor) is the largest group of sensory domains in bacteria, but the dCache-type chemoreceptor that directly binds to formate has not yet been discovered. In this study, formate was identified as a direct-binding ligand of C. jejuni Tlp1 with high sensing specificity. We used the strategy of constructing a functional hybrid receptor of C. jejuni Tlp1 and the Escherichia coli chemoreceptor Tar to screen for the potential ligand of Tlp1, with the binding of formate to Tlp1-LBD being verified using isothermal titration calorimetry. Molecular docking and experimental analyses indicated that formate binds to the membrane-proximal pocket of the dCache subdomain. Chemotaxis assays demonstrated that formate elicits robust attractant responses of the C. jejuni strain NCTC 11168, specifically via Tlp1. The chemoattraction effect of formate via Tlp1 promoted the growth of C. jejuni, especially when competing with Tlp1- or CheY-knockout strains. Our study reveals the molecular mechanisms by which C. jejuni mediates chemotaxis toward formate, and, to our knowledge, is the first report on the high-specificity binding of the dCache-type chemoreceptor to formate as well as the physiological role of chemotaxis toward formate. IMPORTANCE Chemotaxis is important for Campylobacter jejuni to colonize favorable niches in the gastrointestinal tract of its host. However, there is still a lack of knowledge about the ligand molecules for C. jejuni chemoreceptors. The dCache-type chemoreceptor, namely, Tlp1, is the most conserved chemoreceptor in C. jejuni strains; however, the direct-binding ligand(s) triggering chemotaxis has not yet been discovered. In the present study, we found that the ligand that binds directly to Tlp1-LBD with high specificity is formate. C. jejuni exhibits robust chemoattraction toward formate, primarily via Tlp1. Tlp1 is the first reported dCache-type chemoreceptor that specifically binds formate and triggers strong chemotaxis. We further demonstrated that the formate-mediated promotion of C. jejuni growth is correlated with Tlp1-mediated chemotaxis toward formate. Our work provides important insights into the mechanism and physiological function of chemotaxis toward formate and will facilitate further investigations into the involvement of microbial chemotaxis in pathogen-host interactions.

Project description:Campylobacter jejuni is a leading cause of bacterially derived gastroenteritis. A previous mutant screen demonstrated that the heme uptake system (Chu) is required for full colonization of the chicken gastrointestinal tract. Subsequent work identified a PAS domain-containing regulator, termed HeuR, as being required for chicken colonization. Here we confirm that both the heme uptake system and HeuR are required for full chicken gastrointestinal tract colonization, with the heuR mutant being particularly affected during competition with wild-type C. jejuni Transcriptomic analysis identified the chu genes-and those encoding other iron uptake systems-as regulatory targets of HeuR. Purified HeuR bound the chuZA promoter region in electrophoretic mobility shift assays. Consistent with a role for HeuR in chu expression, heuR mutants were unable to efficiently use heme as a source of iron under iron-limiting conditions, and mutants exhibited decreased levels of cell-associated iron by mass spectrometry. Finally, we demonstrate that an heuR mutant of C. jejuni is resistant to hydrogen peroxide and that this resistance correlates to elevated levels of catalase activity. These results indicate that HeuR directly and positively regulates iron acquisition from heme and negatively impacts catalase activity by an as yet unidentified mechanism in C. jejuni IMPORTANCE: Annually, Campylobacter jejuni causes millions of gastrointestinal infections in the United States, due primarily to its ability to reside within the gastrointestinal tracts of poultry, where it can be released during processing and contaminate meat. In the developing world, humans are often infected by consuming contaminated water or by direct contact with livestock. Following consumption of contaminated food or water, humans develop disease that is characterized by mild to severe diarrhea. There is a need to understand both colonization of chickens, to make food safer, and colonization of humans, to better understand disease. Here we demonstrate that to efficiently colonize a host, C. jejuni requires iron from heme, which is regulated by the protein HeuR. Understanding how HeuR functions, we can develop ways to inhibit its function and reduce iron acquisition during colonization, potentially reducing C. jejuni in the avian host, which would make food safer, or limiting human colonization.

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PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis.

Publications

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis.

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