Divergent regulatory pathways control A and S motility in Myxococcus xanthus through FrzE, a CheA-CheY fusion protein.
Myxococcus xanthus moves on solid surfaces by using two gliding motility systems, A motility for individual-cell movement and S motility for coordinated group movements. The frz genes encode chemotaxis homologues that control the cellular reversal frequency of both motility systems. One of the components of the core Frz signal transduction pathway, FrzE, is homologous to both CheA and CheY from the enteric bacteria and is therefore a novel CheA-CheY fusion protein. In this study, we investigated the role of this fusion protein, in particular, the CheY domain (FrzECheY). FrzECheY retains all of the highly conserved residues of the CheY superfamily of response regulators, including Asp709, analogous to phosphoaccepting Asp57 of Escherichia coli CheY. While in-frame deletion of the entire frzE gene caused both motility systems to show a hyporeversal phenotype, in-frame deletion of the FrzECheY domain resulted in divergent phenotypes for the two motility systems: hyperreversals of the A-motility system and hyporeversals of the S-motility system. To further investigate the role of FrzECheY in A and S motility, point mutations were constructed such that the putative phosphoaccepting residue, Asp709, was changed from D to A (and was therefore never subject to phosphorylation) or E (possibly mimicking constitutive phosphorylation). The D709A mutant showed hyperreversals for both motilities, while the D709E mutant showed hyperreversals for A motility and hyporeversal for S motility. These results show that the FrzECheY domain plays a critical signaling role in coordinating A and S motility. On the basis of the phenotypic analyses of the frzE mutants generated in this study, a model is proposed for the divergent signal transduction through FrzE in controlling and coordinating A and S motility in M. xanthus.
Li
Yinuo
Y
Molecular Biology Institute, University of California, Los Angeles, CA 90095-1668, USA.
Bustamante
Víctor H
VH
Lux
Renate
R
Zusman
David
D
Shi
Wenyuan
W
D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000502:physiology*; D002633:Chemotaxis / Q000235:genetics / Q000502:physiology; D003470:Culture Media; D005798:Genes, Bacterial; D009154:Mutation; D016941:Myxococcus xanthus / Q000235:genetics / Q000502:physiology*; D010641:Phenotype; D015398:Signal Transduction
D001426:Bacterial Proteins; D003470:Culture Media
Curr Biol. 2002 Mar 5;12(5):369-77
11882287
Mol Microbiol. 1999 Apr;32(1):1-10
10216854
J Mol Biol. 1993 Jul 5;232(1):67-78
8331671
Mol Microbiol. 2000 Sep;37(6):1357-71
10998168
Mol Microbiol. 1994 Nov;14(4):785-95
7891564
Proc Natl Acad Sci U S A. 1985 Dec;82(24):8767-70
3936045
Mol Microbiol. 1998 Dec;30(5):1123-30
9988486
J Biol Chem. 2002 Mar 22;277(12):9625-8
11779877
Mol Microbiol. 1994 Oct;14(1):61-71
7830561
Proc Natl Acad Sci U S A. 1990 Aug;87(15):5898-902
2165608
Microbiology. 1997 Dec;143 ( Pt 12):3671-82
9421893
Mol Microbiol. 2004 Sep;53(5):1501-13
15387825
J Mol Biol. 1978 Feb 25;119(2):167-78
416222
Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3378-82
8475084
Mol Microbiol. 1995 Feb;15(3):483-94
7783619
J Bacteriol. 2001 Aug;183(16):4786-95
11466282
Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6901-4
11381130
J Bacteriol. 1992 Jul;174(13):4246-57
1624419
Dev Biol. 1978 Jun;64(2):284-96
98366
Nature. 2000 Sep 7;407(6800):98-102
10993081
J Bacteriol. 1990 Sep;172(9):4877-87
2168368
Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):11957-62
9751772
Curr Biol. 2000 Sep 21;10(18):1143-6
10996798
J Bacteriol. 1989 Feb;171(2):819-30
2464581
J Bacteriol. 1982 Jun;150(3):1430-7
6281244
Gene. 1996 Dec 12;183(1-2):153-7
8996101
Mol Microbiol. 1998 Sep;29(5):1249-61
9767592
Proc Natl Acad Sci U S A. 1979 Nov;76(11):5952-6
42906
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5443-8
12704238
Proc Natl Acad Sci U S A. 1975 Feb;72(2):518-22
164657
Mol Microbiol. 1993 Aug;9(3):601-11
8412706
FEBS Lett. 1995 Jan 16;358(1):31-3
7821424