Signal processing in complex chemotaxis pathways

Porter, Steven L.; Wadhams, George H.; Armitage, Judith P.

doi:10.1038/nrmicro2505

Cited by 401 publications

(350 citation statements)

References 135 publications

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“…2). This is likely the reason that even the few bifunctional HKs that have more than one target rarely act on more than two or three downstream RRs (34,38). Monofunctional HKs, however, should act more like kinases in GK loops (Fig.…”

Section: Discussionmentioning

confidence: 99%

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Crosstalk and the evolution of specificity in two-component signaling

Rowland

Deeds

2014

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

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Significance The global architectures of signaling networks in bacteria and eukaryotes are remarkably different: crosstalk between pathways is very common in eukaryotes but is very limited in bacteria. Bacteria use two-component signaling (TCS) to transduce information, relying on a single enzyme to act as both kinase and phosphatase for targets. We used mathematical models to show that introducing crosstalk in TCS always decreases system performance. This indicates that the large-scale differences between eukaryotic and bacterial networks likely derive from differences in the dynamics of the fundamental motifs from which the networks themselves are constructed. We further demonstrated that the pressure to avoid crosstalk has influenced the evolution of new TCS pairs, driving rapid sequence divergence in protein interaction interfaces immediately postduplication.

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Section: Discussionmentioning

confidence: 99%

“…Indeed, there are known examples of HKs that act efficiently on more than one RR (e.g., the bacterial chemotaxis pathway) (38). Although introducing crosstalk does decrease response, the system can compensate by increasing the total expression level of that particular RR to maintain a particular concentration of active RR* (SI Appendix) (3).…”

Section: Discussionmentioning

confidence: 99%

Crosstalk and the evolution of specificity in two-component signaling

Rowland

Deeds

2014

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

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“…2A). Classic chemotaxis systems use CheY as the response regulator downstream of CheA (18). The Chp system has two apparent CheY homologs, PilG and PilH, which have opposite effects on cAMP levels (9).…”

Section: Resultsmentioning

confidence: 99%

Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa

Persat

Inclán

Engel

et al. 2015

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

364

398

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Bacteria have evolved a wide range of sensing systems to appropriately respond to environmental signals. Here we demonstrate that the opportunistic pathogen Pseudomonas aeruginosa detects contact with surfaces on short timescales using the mechanical activity of its type IV pili, a major surface adhesin. This signal transduction mechanism requires attachment of type IV pili to a solid surface, followed by pilus retraction and signal transduction through the Chp chemosensory system, a chemotaxis-like sensory system that regulates cAMP production and transcription of hundreds of genes, including key virulence factors. Like other chemotaxis pathways, pili-mediated surface sensing results in a transient response amplified by a positive feedback that increases type IV pili activity, thereby promoting long-term surface attachment that can stimulate additional virulence and biofilm-inducing pathways. The methyl-accepting chemotaxis protein-like chemosensor PilJ directly interacts with the major pilin subunit PilA. Our results thus support a mechanochemical model where a chemosensory system measures the mechanically induced conformational changes in stretched type IV pili. These findings demonstrate that P. aeruginosa not only uses type IV pili for surface-specific twitching motility, but also as a sensor regulating surface-induced gene expression and pathogenicity.surface sensing | mechanotransduction | type IV pili | virulence N umerous bacterial species exhibit a range of behaviors that are specific to life on surfaces. For many pathogens, surfacespecific phenotypes are often associated with virulent activity, because many infection strategies require contact with a host (1). For example, in Pseudomonas aeruginosa, the type III secretion system, which infects by injecting toxins, requires attachment of individual cells to host-cell membranes (2). The genetic pathways that regulate P. aeruginosa secretion systems have been well characterized (3), but the environmental signals that activate these pathways remain poorly defined (4). Given the requirement for host-cell contact for efficient infection, P. aeruginosa could leverage surface contact as a signal to properly activate and coordinate pathogenicity. Indeed, our laboratory recently demonstrated that prolonged association with a solid surface contributes to P. aeruginosa pathogenicity when bacteria and host cells are forced together (5). Here we address the fundamental question of how bacteria rapidly sense surface contact and transduce this input into a cellular response over short timescales.Surface-specific behaviors require intimate contact between cells and substrate. In P. aeruginosa, contact is mediated by several adhesins, particularly type IV pili (TFP). TFP are long, motorized fimbriae that also provide cells with surface-specific twitching motility and are essential to virulence and biofilm formation (6, 7). Successive TFP extension, attachment, and retraction promote intimate association with surfaces and motility along them. Because TFP dynamically int...

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“…Analysis of the M. gryphiswaldense genome for genes that might encode proteins involved in aerotaxis revealed at least 56 genes encoding putative chemoreceptors 20 , known as methyl-accepting chemotaxis proteins (MCPs) (Supplementary Table 3), and four putative chemotaxis operons designated cheOp1-4 (Fig. 4).…”

Section: Resultsmentioning

confidence: 99%

“…Chemotactic signal transduction in all bacteria is based on two-component systems involving autophosphorylation of the histidine kinase, CheA, followed by subsequent phosphotransfer to a response regulator, CheY 20 . We found that of the ARTICLE four identified chemotaxis operons of M. gryphiswaldense, only cheOp1, comprising the canonical set of chemotaxis genes (cheAWYBR), is involved in aerotaxis and swimming polarity (Fig.…”

Section: Discussionmentioning

confidence: 99%