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A Quantitative Model of the Switch Cycle of an Archaeal Flagellar Motor and its Sensory Control

Torsten Nutsch ^*, Dieter Oesterhelt , Ernst Dieter Gilles ^* and Wolfgang Marwan 

^* Max-Planck-Institute for Dynamics of Complex Technical Systems, Magdeburg, Germany; Max-Planck-Institute for Biochemistry, Martinsried, Germany; and Science and Technology Research Institute, University of Hertfordshire, Hatfield, United Kingdom

Correspondence: Address reprint requests to Wolfgang Marwan, Max-Planck-Institute for Dynamics of Complex Technical Systems and Institute for Biology, Otto-von-Guericke-University Magdeburg, Sandtorstrasse 1, 39106 Magdeburg, Germany. Tel.: 49-6110-410; E-mail: marwan{at}mpi-magdeburg.mpg.de.

By reverse-engineering we have detected eight kinetic phases of the symmetric switch cycle of the Halobacterium salinarum flagellar motor assembly and identified those steps in the switch cycle that are controlled by sensory rhodopsins during phototaxis. Upon switching the rotational sense, the flagellar motor assembly passes through a stop state from which all subunits synchronously resume rotation in the reverse direction. The assembly then synchronously proceeds through three subsequent functional states of the switch: Refractory, Competent, and Active, from which the rotational sense is switched again. Sensory control of the symmetric switch cycle occurs at two steps in each rotational sense by inversely regulating the probabilities for a change from the Refractory to the Competent and from Competent to the Active rotational mode. We provide a mathematical model for flagellar motor switching and its sensory control, which is able to explain all tested experimental results on spontaneous and light-controlled motor switching, and give a mechanistic explanation based on synchronous conformational transitions of the subunits of the switch complex after reversible dissociation and binding of a response regulator (CheYP). We conclude that the kinetic mechanism of flagellar motor switching and its sensory control is fundamentally different in the archaeon H. salinarum and the bacterium Escherichia coli.