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J. Biol. Chem., Vol. 277, Issue 2, 1593-1598, January 11, 2002

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Sensing of Cytoplasmic pH by Bacterial Chemoreceptors Involves the Linker Region That Connects the Membrane-spanning and the Signal-modulating Helices^*

Tohru Umemura^§, Yumi Matsumoto, Kouhei Ohnishi^¶, Michio Homma, and Ikuro Kawagishi^**

From the  Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602 and ^¶ Kamaishi Laboratory, Marine Biotechnology Institute, Kamaishi, Iwate 026-0001, Japan

The two major chemoreceptors of Escherichia coli, Tsr and Tar, mediate opposite responses to the same changes in cytoplasmic pH (pH_i). We set out to identify residues involved in pH_i sensing to gain insight into the general mechanisms of signaling employed by the chemoreceptors. Characterization of various chimeras of Tsr and Tar localized the pH_i-sensing region to Arg²⁵⁹-His²⁶⁷ of Tar and Gly²⁶¹-Asp²⁶⁹ of Tsr. This region of Tar contains three charged residues (Arg²⁵⁹-Ser²⁶¹, Asp²⁶³, and His²⁶⁷) that have counterparts of opposite charge in Tsr (Gly²⁶¹-Glu²⁶², Arg²⁶⁵, and Asp²⁶⁹). The replacement of all of the three charged residues in Tar or Arg²⁵⁹-Ser²⁶⁰ alone by the corresponding residues of Tsr reversed the polarity of pH_i response, whereas the replacement of Asp²⁶³ or His²⁶⁷ did not change the polarity but altered the time course of pH_i response. These results suggest that the electrostatic properties of a short cytoplasmic region within the linker region that connects the second transmembrane helix to the first methylation helix is critical for switching the signaling state of the chemoreceptors during pH sensing. Similar conformational changes of this region in response to external ligands may be critical components of transmembrane signaling.

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