Two different <i>Pseudomonas aeruginosa</i> chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase

Güvener, Zehra Tüzün; Tifrea, Delia F.; Harwood, Caroline S.

doi:10.1111/j.1365-2958.2006.05218.x

Cited by 85 publications

(105 citation statements)

References 38 publications

(54 reference statements)

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“…In E. coli, the concentration of individual chemoreceptors within the chemoreceptor arrays is variable and affects signaling (25). Changes in the chemoreceptor content have been reported in Pseudomonas aeruginosa (26) and Rhodobacter sphaeroides (27); however, the effect of such changes on chemotaxis has not been established. Here we presented a case where changes in the chemoreceptor content dramatically affect motile behavior under very specific conditions: chemosensory input to AerC (changes in redox homeostasis) acts as a major cue to modulate behavior under nitrogen-fixing conditions.…”

Section: Discussionmentioning

confidence: 99%

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

Xie¹,

Ulrich

Zhulin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

107

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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...

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Section: Discussionmentioning

confidence: 99%

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

Xie¹,

Ulrich

Zhulin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

107

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“…We next asked whether receptor proteins form one single, heterologous cluster or whether they have separate and distinct subcellular localizations, as observed for P. aeruginosa (11). We introduced mcpX fused to the mRFP gene into the genomes of strains expressing McpU-, McpZ-, or IcpA-EGFP fusions (Table 1).…”

Section: Resultsmentioning

confidence: 99%

“…P. aeruginosa locates both systems, Che and Che2, at the cell poles; however, they are expressed at different phases of growth. McpA, for example, is expressed during stationary phase and joins the existing Che protein complex at the cell poles (11).…”

Section: Discussionmentioning

confidence: 99%

Cellular Localization of Predicted Transmembrane and Soluble Chemoreceptors in Sinorhizobium meliloti

Meier

Scharf

2009

J Bacteriol

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The chemosensory machinery of Escherichia coli and other bacteria is arranged in large protein clusters (22,28,43,49). One individual signaling unit is formed by a ternary assembly of chemoreceptor dimers, the histidine kinase CheA, and the so-called adaptor protein CheW. E. coli cells contain 20,000 receptor molecules (22). Recent studies suggest that the stoichiometry of such chemosensory complexes is flexible (17, 32). Allosteric interactions among receptors in a chemosensory cluster facilitate amplification and integration of chemotactic stimuli (20,21,41,42).In contrast to E. coli, which has a single set of che genes and only five receptors, some species from the alpha subgroup of the proteobacteria, such as Pseudomonas aeruginosa, Rhodobacter sphaeroides, and Sinorhizobium meliloti, encode multiple chemotaxis-like systems, reflecting their complex lifestyle. The opportunistic pathogen P. aeruginosa possesses four chemotaxis systems that together have 26 known receptor genes (47), while the nonsulfur bacterium R. sphaeroides has three separate che operons with 13 known receptor-like genes (27).The symbiotic soil bacterium S. meliloti possesses eight methyl-accepting chemotaxis proteins (MCPs), McpS to McpZ, and one transducer-like-protein, IcpA, which lacks the conserved Glu or Gln residues that serve as methyl-accepting sites (29). Seven of the MCP proteins are localized in the cytoplasmic membrane via two membrane-spanning regions, whereas McpY and IcpA lack such hydrophobic regions. The S. meliloti mcpS gene is the third gene of the che2 operon located on the symbiotic plasmid pSymA (4). The icpA gene is the first gene of the chromosomal che operon comprising a total of 10 genes (9). This operon is part of the flagellar gene cluster with 56 chemotaxis, motor, and flagellar genes residing on one contiguous 51.4-kb chromosomal region (7, 46). For bacteria with numerous chemoreceptor genes, it is not unusual to find most of them located outside chemotaxis operons. This is the case with six monocistronic S. meliloti mcp genes which are scattered throughout the genome. The remaining mcpW gene is cotranscribed with a putative cheW gene. In this study, we examined the localization of the nine receptor gene products in the S. meliloti cell by fluorescence microscopy in wildtype and various deletion strains. The cellular localization of the two soluble receptors, McpY and IcpA, was also analyzed in vitro using an immunoblot assay on fractionated cell components. Furthermore, timing of chemoreceptor gene expression during exponential and stationary phase was determined. MATERIALS AND METHODSBacterial strains and plasmids. Derivatives of E. coli K-12 and S. meliloti MV II-1 (16) and the plasmids used are listed in Table 1.Media and growth conditions. E. coli strains were grown in Luria broth (23) at 37°C. S. meliloti strains were grown in TYC medium (0.5% tryptone, 0.3% yeast extract, 0.13% CaCl 2 ⅐ 6H 2 O [pH 7.0] at 30°C) (37). Cells for fluorescence microscopy were grown for 2 days in TYC medium, first diluted 1...

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“…In this respect, several parallels to Pseudomonas aeruginosa exist. Two of its four chemotaxis gene clusters are involved in the che and che2 chemotaxis pathways (13). Data suggest that, in analogy to R. sphaeroides, the transmembrane receptors signal into the che pathway, whereas the soluble Aer-2/McpB chemoreceptor signals into the che2 pathway.…”

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confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase

Abstract: SummaryPseudomonas aeruginosa has sets of sensory genes designated che and che2.

Cited by 85 publications

References 38 publications

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis

Cellular Localization of Predicted Transmembrane and Soluble Chemoreceptors in Sinorhizobium meliloti

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

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