Role of Proton Motive Force in Sensory Transduction in Bacteria

Taylor, Barry

doi:10.1146/annurev.mi.37.100183.003003

Cited by 100 publications

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“…Aerotaxis, the behavioral response to oxygen, requires a functional electron transport system (2). Oxygen stimulates electron transport through the electron transport system, increasing the proton motive force (2,3). A postulated aerotaxis-transducing protein responds to the increase in electron transport͞proton motive force and initiates a signal for the behavioral response to oxygen (3)(4)(5)(6).…”

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confidence: 99%

“…Oxygen stimulates electron transport through the electron transport system, increasing the proton motive force (2,3). A postulated aerotaxis-transducing protein responds to the increase in electron transport͞proton motive force and initiates a signal for the behavioral response to oxygen (3)(4)(5)(6). Chemicals other than oxygen that stimulate electron transport also elicit an aerotaxis-like behavioral response in bacteria (5,7,8).…”

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confidence: 99%

“…The aerotaxis transducer may mediate other types of bacterial behavior, such as the newly described taxis to a preferred redox potential (9) and energy taxis to carbon sources, such as glycerol (10) or proline (11). Each of these behaviors involves modulation of the proton motive force and electron transport as the initial sensory transduction event (3).…”

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confidence: 99%

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The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior

Rebbapragada

Johnson

Harding

et al. 1997

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

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We identified a protein, Aer, as a signal transducer that senses intracellular energy levels rather than the external environment and that transduces signals for aerotaxis (taxis to oxygen) and other energy-dependent behavioral responses in Escherichia coli. Domains in Aer are similar to the signaling domain in chemotaxis receptors and the putative oxygen-sensing domain of some transcriptional activators. A putative FAD-binding site in the N-terminal domain of Aer shares a consensus sequence with the NifL, Bat, and Wc-1 signal-transducing proteins that regulate gene expression in response to redox changes, oxygen, and blue light, respectively. A double mutant deficient in aer and tsr, which codes for the serine chemoreceptor, was negative for aerotaxis, redox taxis, and glycerol taxis, each of which requires the proton motive force and͞or electron transport system for signaling. We propose that Aer and Tsr sense the proton motive force or cellular redox state and thereby integrate diverse signals that guide E. coli to environments where maximal energy is available for growth.

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confidence: 99%

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The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior

Rebbapragada

Johnson

Harding

et al. 1997

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

Self Cite

257

349

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“…4A). The reduction in energy levels of the cells can be induced by the addition of chemical compounds, such as the protonophore CCCP, which dissipates the proton-motive force generated in the cytoplasmic membrane, provoking energy stress as the result of intracellular ATP depletion (35). To test the sensitivity of the ⌬pph2 mutant to CCCP during growth, the WT strain and the mutant were inoculated into liquid CTT containing several concentrations of the protonophore, and the A 600 after 24-h incubation was monitored.…”

Section: Analysis Of the Pph2 Sequence And Expression Of The Gene-mentioning

confidence: 99%

Myxococcus xanthus Pph2 Is a Manganese-dependent Protein Phosphatase Involved in Energy Metabolism

García-Hernández

Moraleda‐Muñoz

Castañeda-García

et al. 2009

Journal of Biological Chemistry

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The multicellular behavior of the myxobacterium Myxococcus xanthus requires the participation of an elevated number of signal-transduction mechanisms to coordinate the cell movements and the sequential changes in gene expression patterns that lead to the morphogenetic and differentiation events. These signaltransduction mechanisms are mainly based on two-component systems and on the reversible phosphorylation of protein targets mediated by eukaryotic-like protein kinases and phosphatases. Among all these factors, protein phosphatases are the elements that remain less characterized. Hence, we have studied in this work the physiological role and biochemical activity of the protein phosphatase of the family PPP (phosphoprotein phosphatases) designated as Pph2, which is forming part of the same operon as the two-component system phoPR1. We have demonstrated that this operon is induced upon starvation in response to the depletion of the cell energy levels. The increase in the expression of the operon contributes to an efficient use of the scarce energy resources available for developing cells to ensure the completion of the life cycle. In fact, a ⌬pph2 mutant is defective in aggregation, sporulation yield, morphology of the myxospores, and germination efficiency. The yeast two-hybrid technology has shown that Pph2 interacts with the gene products of MXAN_1875 and 5630, which encode a hypothetical protein and a glutamine synthetase, respectively. Because Pph2 exhibits Ser/Thr, and to some extent Tyr, Mn 2؉ -dependent protein phosphatase activity, it is expected that this function is accomplished by dephosphorylation of the specific protein substrates.Myxococcus xanthus is a soil-dwelling ␦-Proteobacterium that undergoes a life cycle unique among the prokaryotes. During growth, cells form predatory communities known as swarms, which feed cooperatively. Upon starvation, cells initiate a multicellular developmental program that culminates with the formation of macroscopic fruiting bodies filled with resistant myxospores. The spores remain dormant until nutrients are available again, when they germinate and initiate a new vegetative cycle (1). This complex lifestyle forces the cells not only to scrutinize all the changes in their environment, but also to maintain a precise communication with each other to coordinate their movement and behavior. In fact, signal-transduction mechanisms of diverse nature have been reported to function in the cell synchronization required during development (2, 3). One of these mechanisms is based on eukaryotic-like protein kinases (ELKs), 3 which originate phosphoesters on Ser/ Thr/Tyr residues. Thus, the myxobacterial kinome is the largest one among the prokaryotes, which seems to correlate with their multicellular behavior (4). The presence of ELKs implies the need of protein phosphatases (PPs) to revert the action of the kinases. These two types of proteins will function together to switch on and off the signal-transduction pathways where they participate by their opposite action on speci...

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“…Over the years there has been speculation as to whether the signal for so-called 'energy taxis' might be a change in the p, via a 'protometer' sensing changes in the proton motive force directly (Taylor 1983;Glagolev 1984), or a change in rate of electron transfer, i.e., a redox sensor. In E. coli aerotactic behavior is signaled primarily via the Aer protein, which has the C-terminal domain of a membrane-spanning chemosensory MCP (Bibikov et al 1997(Bibikov et al , 2000Rebbapragada et al 1997) and an FAD-binding PAS domain at the N-terminus.…”

Section: Rhodobacter Sphaeroidesmentioning

confidence: 99%

Light-induced behavioral responses (‘phototaxis’) in prokaryotes

Armitage

Hellingwerf

Discoveries in Photosynthesis

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Light-induced sensory responses are among the oldest scientific observations on bacterial behavior. Various types of response have been characterized physiologically in detail. However, the molecular basis of this type of response is only slowly emerging. In many of these systems photosynthetic pigments absorb the light. This then generates a signal via electron transport, feeding into a canonical chemotaxis signal transduction pathway. Nevertheless, several examples have been identified in which dedicated photoreceptor proteins do play a role. The intrinsic complexity of some of these signal transduction systems is overwhelming, in part because of the significant apparent redundancy. The genomics information that is now available for several model organisms (in particular Rhodobacter sphaeroides and Synechocystis sp. PCC6803) facilitates obtaining an increasingly detailed view of the molecular basis of the partial reactions that jointly form the basis of this type of elementary behavioral response.

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Role of Proton Motive Force in Sensory Transduction in Bacteria

Cited by 100 publications

References 0 publications

The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior

The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior

Myxococcus xanthus Pph2 Is a Manganese-dependent Protein Phosphatase Involved in Energy Metabolism

Light-induced behavioral responses (‘phototaxis’) in prokaryotes

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