A cyclic di-GMP-binding adaptor protein interacts with a chemotaxis methyltransferase to control flagellar motor switching.
The bacterial messenger cyclic diguanylate monophosphate (c-di-GMP) binds to various effectors, the most common of which are single-domain PilZ proteins. These c-di-GMP effectors control various cellular functions and multicellular behaviors at the transcriptional or posttranslational level. We found that MapZ (methyltransferase-associated PilZ; formerly known as PA4608), a single-domain PilZ protein from the opportunistic pathogen Pseudomonas aeruginosa, directly interacted with the methyltransferase CheR1 and that this interaction was enhanced by c-di-GMP. In vitro assays indicated that, in the presence of c-di-GMP, MapZ inhibited CheR1 from methylating the chemoreceptor PctA, which would be expected to increase its affinity for chemoattractants and promote chemotaxis. MapZ localized to the poles of P. aeruginosa cells, where the flagellar motor and other chemotactic proteins, including PctA and CheR1, are also located. P. aeruginosa cells exhibit a random walk behavior by frequently switching the direction of flagellar rotation in a uniform solution. We showed that binding of c-di-GMP to MapZ decreased the frequency of flagellar motor switching and that MapZ was essential for generating the heterogeneous motility typical of P. aeruginosa cell populations and for efficient surface attachment during biofilm formation. Collectively, the studies revealed that c-di-GMP affects flagellar motor output by regulating the methylation of chemoreceptors through a single-domain PilZ adaptor protein.
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.|Guangdong Innovative and Entrepreneurial Research Team of Sociomicrobiology Basic Science and Frontier Technology, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou 510642, China.
Linghui
L
Xu
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.
Lingyi
L
Xin
Bioinformatics Institute, Agency for Science, Technology and Research (A*STAR), 30 Biopolis Street, #07-01, Singapore 138671, Singapore.
Yukai
Y
Zeng
Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.|Interdisciplinary Graduate School, Nanyang Technological University, Singapore 637551, Singapore.
Joey Kuok Hoong
JK
Yam
Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.|Interdisciplinary Graduate School, Nanyang Technological University, Singapore 637551, Singapore.
Yichen
Y
Ding
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.
Prabhadevi
P
Venkataramani
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.
Qing Wei
QW
Cheang
Guangdong Innovative and Entrepreneurial Research Team of Sociomicrobiology Basic Science and Frontier Technology, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou 510642, China.
Xiaobei
X
Yang
Institute of Molecular and Cell Biology, A*STAR, 61 Biopolis Drive, Singapore 138673, Singapore.
Xuhua
X
Tang
Integrative Microbiology Research Centre, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou 510642, China.
Lian-Hui
LH
Zhang
Bioinformatics Institute, Agency for Science, Technology and Research (A*STAR), 30 Biopolis Street, #07-01, Singapore 138671, Singapore.
Keng-Hwee
KH
Chiam
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore. zxliang@ntu.edu.sg yangliang@ntu.edu.sg.|Singapore Centre for Environmental Life Sciences Engineering, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore.
Liang
L
Yang
School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551, Singapore. zxliang@ntu.edu.sg yangliang@ntu.edu.sg.
Zhao-Xun
ZX
Liang
D048868:Adaptor Proteins, Signal Transducing / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D002633:Chemotaxis / Q000502:physiology*; D006152:Cyclic GMP / Q000031:analogs & derivatives* / Q000235:genetics / Q000378:metabolism; D005407:Flagella / Q000235:genetics / Q000378:metabolism*; D008780:Methyltransferases / Q000235:genetics / Q000378:metabolism*; D011550:Pseudomonas aeruginosa / Q000235:genetics / Q000378:metabolism*
D048868:Adaptor Proteins, Signal Transducing; D001426:Bacterial Proteins; C062025:bis(3',5')-cyclic diguanylic acid; D008780:Methyltransferases; D006152:Cyclic GMP