Signal Processing and Flagellar Motor Switching During Phototaxis of Halobacterium salinarum

Abstract

Prokaryotic taxis, the active search of motile cells for the best environmental conditions, is one of the paradigms for signal transduction. The search algorithm implemented by the cellular biochemistry modulates the probability of switching the rotational direction of the flagellar motor, a nanomachine that propels prokaryotic cells. On the basis of the well-known biochemical mechanisms of chemotaxis in Escherichia coli, kinetic modeling of the events leading from chemoreceptor activation by ligand binding to the motility response has been performed with great success. In contrast to Escherichia coli, Halobacterium salinarum, in addition, responds to visible light, which is sensed through specific photoreceptors of different wavelength sensitivity (phototaxis). Light stimuli of defined intensity and time course can be controlled precisely, which facilitates input-output measurements used for system analysis of the molecular network connecting the sensory receptors to the flagellar motor switch. Here, we analyze the response of halobacterial cells to single and double-pulse light stimuli and present the first kinetic model for prokaryotic cells that couples the signal-transduction pathway with the flagellar motor switch. Modeling based on experimental data supports the current biochemical model of halobacterial phototaxis. Moreover, the simulations demonstrate that motor switching occurs through subsequent rate-limiting steps, which are both under sensory control, suggesting that two signals may be involved in halobacterial phototaxis

Bacterial PEP-Dependent Carbohydrate: Phosphotransferase Systems Couple Sensing and Global Control Mechanisms

“…diffusion limitations for proteins within the cell [52], or when they indicate major deviations between in vitro and in vivo data. Typical examples for this approach are the modeling of the control of glucose metabolism by EII Glc [73,74], of phototaxis in Halobacterium salinarum [75], and, hopefully, of the precise role the complex phosphorylation cycle of EI does play in PTS-dependent chemosensing [53].…”

Archaeal Flagella, Bacterial Flagella and Type IV Pili: A Comparison of Genes and Posttranslational Modifications

“…These include proteins involved in signal recognition and transduction (methyl-accepting chemotaxis proteins or MCPs, CheD), excitation (CheA, CheW, CheY), adaptation (CheR, CheB) and signal removal (CheC, CheX) [Szurmant and Ordal, 2004]. Notably, the cells contain one or more genes annotated as CheY although in bacteria this response regulator delivers its signal via interaction with the flagellar switch protein FliM located at the base of the flagellum and so far no homologue to FliM has yet been reported in archaea [Faguy and Jarrell, 1999;Nutsch et al, 2003b]. To date, how CheY delivers its signal to the archaeal flagellum is a mystery.…”

“…This includes three species of Methanosarcina in which flagella and/or motility have never been reported. However, another species of Methanosarcina , M. baltica , can be flagellated [Singh et al, 2005] Kalmokoff and Jarrell, 1991;Nagahisa et al, 1999;Nutsch et al, 2003a;Serganova et al, 2002;Thomas and Jarrell, 2001 [Kurr et al, 1991] and P. aerophilum [Volkl et al, 1993] have been reported to be motile. N. equitans has never been reported to be motile although it does have some sort of appendage [Waters et al, 2003].…”

“…At the genetic level, chemotaxis in archaea has been best studied in H. salinarum where deletion analysis of the che operon has led to insights into functions of the various proteins in archaea and contributed to knowledge about the switch [Kokoeva et al, 2002;Nutsch et al, 2003bNutsch et al, , 2005Rudolph and Oesterhelt, 1996]. Interestingly, H. salinarum cells alternate between forward and reverse swimming as determined by CW and CCW rotation of their right-handed flagella, in contrast to most bacteria, like E. coli, which alternate between forward swimming (CCW rotation of left-handed flagella) and tumbling (CW rotation of left-handed flagella).…”

Cell Surface Structures of Archaea

“…Many archaea are known to be chemotactic and/or phototactic (38,60,68). The ability of archaea to respond to changes in their environment is through a system very similar to the chemotaxis system found in bacteria.…”