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Multiple signals modulate the activity of the complex sensor kinase TodS.

Silva-Jiménez H, Ortega Á, García-Fontana C, Ramos JL, Krell T - Microb Biotechnol (2014)

Bottom Line: In the presence of toluene, menadione reduced TodS activity whereas toluene did not stimulate activity in the presence of menadione.The opposing effects of menadione on glucose and toluene metabolism may be partially responsible for the interwoven regulation of both catabolic pathways.This work provides mechanistic detail on how complex sensor kinases integrate different types of signal molecules.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Protection, Consejo Superior de Investigaciones Científicas, Estación Experimental del Zaidín, C/ Prof. Albareda 1, Granada, 18008, Spain.

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Schematic representation of the domain organization and mode of action of the TodS/TodT TCS. The phosphorylgroup-accepting residues and the phosphorelay are indicated as established by Busch and colleagues (2009). PAS, Per-Arnt-Sim-type sensor domain; DHp, dimerization/histidine phosphotransfer domain; Ca, catalytic domain; RRR, response regulator receiver domain; DNA-b, DNA-binding domain; P, phosphorylgroup.
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fig01: Schematic representation of the domain organization and mode of action of the TodS/TodT TCS. The phosphorylgroup-accepting residues and the phosphorelay are indicated as established by Busch and colleagues (2009). PAS, Per-Arnt-Sim-type sensor domain; DHp, dimerization/histidine phosphotransfer domain; Ca, catalytic domain; RRR, response regulator receiver domain; DNA-b, DNA-binding domain; P, phosphorylgroup.

Mentions: We have addressed this question using the complex TodS/TodT TCS of Pseudomonas putida DOT-T1E, which was shown to modulate the expression from promoter PtodX that controls the genes of the toluene dioxygenase pathway (TOD) for the metabolization of benzene, toluene and ethylbenzene (Zylstra and Gibson, 1989; Lau et al., 1997; Mosqueda et al., 1999). The 108 kDa sensor kinase TodS is composed of two transmitter modules each comprising a dimerization/histidine phosphotransfer domain and a catalytic domain (Fig. 1). Each transmitter module is preceded by a Per-Arnt-Sim (PAS) domain, and a receiver domain is found in the centre of the TodS sequence. We have shown previously that TOD pathway expression is induced by a range of aromatic compounds like toluene (Lacal et al., 2006) and have demonstrated that these effectors bind to the N-terminal PAS domain, increasing the activity of the N-terminal autokinase module (Lacal et al., 2006; Busch et al., 2009). In addition to these agonists, we have identified structurally very similar compounds (o-xylene, for example) that also bind to the N-terminal PAS domain, but do not stimulate TodS autophosphorylation (Busch et al., 2007). The presence of these compounds (termed antagonists) was found to reduce the magnitude of agonist-mediated upregulation (Busch et al., 2007). The TodS phosphorylation state is thus controlled by the concerted action of agonists and antagonists that compete for the same site at TodS. Similar observations were made for the homologous system TmoS/TmoT that controls the toluene-4-monooxygenase degradation pathway in Pseudomonas mendocina (Silva-Jimenez et al., 2012). We were also able to show that TodS operates by a His1-Asp1-His2-Asp2 phosphorelay mechanism (Busch et al., 2007; 2009) (Fig. 1). TodS lacks transmembrane regions and can be obtained as soluble and active protein (Lacal et al., 2006).


Multiple signals modulate the activity of the complex sensor kinase TodS.

Silva-Jiménez H, Ortega Á, García-Fontana C, Ramos JL, Krell T - Microb Biotechnol (2014)

Schematic representation of the domain organization and mode of action of the TodS/TodT TCS. The phosphorylgroup-accepting residues and the phosphorelay are indicated as established by Busch and colleagues (2009). PAS, Per-Arnt-Sim-type sensor domain; DHp, dimerization/histidine phosphotransfer domain; Ca, catalytic domain; RRR, response regulator receiver domain; DNA-b, DNA-binding domain; P, phosphorylgroup.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4321377&req=5

fig01: Schematic representation of the domain organization and mode of action of the TodS/TodT TCS. The phosphorylgroup-accepting residues and the phosphorelay are indicated as established by Busch and colleagues (2009). PAS, Per-Arnt-Sim-type sensor domain; DHp, dimerization/histidine phosphotransfer domain; Ca, catalytic domain; RRR, response regulator receiver domain; DNA-b, DNA-binding domain; P, phosphorylgroup.
Mentions: We have addressed this question using the complex TodS/TodT TCS of Pseudomonas putida DOT-T1E, which was shown to modulate the expression from promoter PtodX that controls the genes of the toluene dioxygenase pathway (TOD) for the metabolization of benzene, toluene and ethylbenzene (Zylstra and Gibson, 1989; Lau et al., 1997; Mosqueda et al., 1999). The 108 kDa sensor kinase TodS is composed of two transmitter modules each comprising a dimerization/histidine phosphotransfer domain and a catalytic domain (Fig. 1). Each transmitter module is preceded by a Per-Arnt-Sim (PAS) domain, and a receiver domain is found in the centre of the TodS sequence. We have shown previously that TOD pathway expression is induced by a range of aromatic compounds like toluene (Lacal et al., 2006) and have demonstrated that these effectors bind to the N-terminal PAS domain, increasing the activity of the N-terminal autokinase module (Lacal et al., 2006; Busch et al., 2009). In addition to these agonists, we have identified structurally very similar compounds (o-xylene, for example) that also bind to the N-terminal PAS domain, but do not stimulate TodS autophosphorylation (Busch et al., 2007). The presence of these compounds (termed antagonists) was found to reduce the magnitude of agonist-mediated upregulation (Busch et al., 2007). The TodS phosphorylation state is thus controlled by the concerted action of agonists and antagonists that compete for the same site at TodS. Similar observations were made for the homologous system TmoS/TmoT that controls the toluene-4-monooxygenase degradation pathway in Pseudomonas mendocina (Silva-Jimenez et al., 2012). We were also able to show that TodS operates by a His1-Asp1-His2-Asp2 phosphorelay mechanism (Busch et al., 2007; 2009) (Fig. 1). TodS lacks transmembrane regions and can be obtained as soluble and active protein (Lacal et al., 2006).

Bottom Line: In the presence of toluene, menadione reduced TodS activity whereas toluene did not stimulate activity in the presence of menadione.The opposing effects of menadione on glucose and toluene metabolism may be partially responsible for the interwoven regulation of both catabolic pathways.This work provides mechanistic detail on how complex sensor kinases integrate different types of signal molecules.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Protection, Consejo Superior de Investigaciones Científicas, Estación Experimental del Zaidín, C/ Prof. Albareda 1, Granada, 18008, Spain.

Show MeSH
Related in: MedlinePlus