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Journal of Bacteriology, December 2005, p. 8403-8410, Vol. 187, No. 24
0021-9193/05/$08.00+0     doi:10.1128/JB.187.24.8403-8410.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Only One of the Five CheY Homologs in Vibrio cholerae Directly Switches Flagellar Rotation

Akihiro Hyakutake,¹ Michio Homma,¹ Melissa J. Austin,³ Markus A. Boin,³ Claudia C. Häse,³ and Ikuro Kawagishi^1,2*

Division of Biological Science, Graduate School of Science,¹ Institute for Advanced Research, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan,² Department of Microbiology, Oregon State University, 220 Nash Hall, Corvallis, Oregon 97331³

Received 4 August 2004/ Accepted 15 September 2005

Vibrio cholerae has three sets of chemotaxis (Che) proteins, including three histidine kinases (CheA) and four response regulators (CheY) that are encoded by three che gene clusters. We deleted the cheY genes individually or in combination and found that only the cheY3 deletion impaired chemotaxis, reinforcing the previous conclusion that che cluster II is involved in chemotaxis. However, this does not exclude the involvement of the other clusters in chemotaxis. In other bacteria, phospho-CheY binds directly to the flagellar motor to modulate its rotation, and CheY overexpression, even without CheA, causes extremely biased swimming behavior. We reasoned that a V. cholerae CheY homolog, if it directly controls flagellar rotation, should also induce extreme swimming behavior when overproduced. This was the case for CheY3 (che cluster II). However, no other CheY homolog, including the putative CheY (CheY0) protein encoded outside the che clusters, affected swimming, demonstrating that these CheY homologs cannot act directly on the flagellar motor. CheY4 very slightly enhanced the spreading of an Escherichia coli cheZ mutant in semisolid agar, raising the possibility that it can affect chemotaxis by removing a phosphoryl group from CheY3. We also found that V. cholerae CheY3 and E. coli CheY are only partially exchangeable. Mutagenic analyses suggested that this may come from coevolution of the interacting pair of proteins, CheY and the motor protein FliM. Taken together, it is likely that the principal roles of che clusters I and III as well as cheY0 are to control functions other than chemotaxis.

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* Corresponding author. Mailing address: Division of Biological Science, Graduate School of Science, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan. Phone: 81 52 789 2993. Fax: 81 52 789 3001. E-mail: i45406a{at}cc.nagoya-u.ac.jp.

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Journal of Bacteriology, December 2005, p. 8403-8410, Vol. 187, No. 24
0021-9193/05/$08.00+0     doi:10.1128/JB.187.24.8403-8410.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

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