Cyclic di-GMP differentially tunes a bacterial flagellar motor through a novel class of CheY-like regulators

ELife
Jutta NesperUrs Jenal

Abstract

The flagellar motor is a sophisticated rotary machine facilitating locomotion and signal transduction. Owing to its important role in bacterial behavior, its assembly and activity are tightly regulated. For example, chemotaxis relies on a sensory pathway coupling chemical information to rotational bias of the motor through phosphorylation of the motor switch protein CheY. Using a chemical proteomics approach, we identified a novel family of CheY-like (Cle) proteins in Caulobacter crescentus, which tune flagellar activity in response to binding of the second messenger c-di-GMP to a C-terminal extension. In their c-di-GMP bound conformation Cle proteins interact with the flagellar switch to control motor activity. We show that individual Cle proteins have adopted discrete cellular functions by interfering with chemotaxis and by promoting rapid surface attachment of motile cells. This study broadens the regulatory versatility of bacterial motors and unfolds mechanisms that tie motor activity to mechanical cues and bacterial surface adaptation.

References

Jan 1, 1991·Methods in Enzymology·B Ely
Oct 25, 1990·Nucleic Acids Research·T D Schneider, R M Stephens
Sep 1, 1989·Proceedings of the National Academy of Sciences of the United States of America·A J Wolfe, H C Berg
Feb 15, 1984·Journal of Molecular Biology·S Koyasu, Y Shirakihara
Jul 1, 1982·Journal of Bacteriology·J S Parkinson, S E Houts
Oct 1, 1993·Proceedings of the National Academy of Sciences of the United States of America·M WelchM Eisenbach
Sep 1, 1997·Nucleic Acids Research·S F AltschulD J Lipman
Feb 21, 1998·Proceedings of the National Academy of Sciences of the United States of America·B E ScharfH C Berg
Apr 16, 1998·Proceedings of the National Academy of Sciences of the United States of America·M BurkartR M Harshey
May 20, 1998·Proceedings of the National Academy of Sciences of the United States of America·G KarimovaD Ladant
Mar 25, 2000·Journal of Molecular Biology·H S ChoJ G Pelton
Mar 22, 2001·Proceedings of the National Academy of Sciences of the United States of America·W C NiermanJ Eisen
Oct 24, 2001·Biochemistry·S Kojima, D F Blair
Mar 8, 2003·Molecular Microbiology·Phillip AldridgeUrs Jenal
Oct 7, 2003·Annual Review of Microbiology·Rasika M Harshey
May 15, 2004·Environmental Microbiology·Michael Y Galperin
Jun 3, 2004·Genome Research·Gavin E CrooksSteven E Brenner
Apr 12, 2005·Molecular Microbiology·Ursula AttmannspacherRüdiger Schmitt
May 13, 2005·The EMBO Journal·Qingfeng WangRasika M Harshey
Sep 5, 2006·The Journal of Biological Chemistry·Steven L PorterJudith P Armitage
Mar 16, 2007·Proceedings of the National Academy of Sciences of the United States of America·Matthias ChristenUrs Jenal
Oct 19, 2007·PLoS Genetics·Hany S GirgisSaeed Tavazoie
Jan 1, 2008·Trends in Biochemical Sciences·Gerald L HazelbauerJohn S Parkinson
May 17, 2008·Nature Reviews. Microbiology·Fabienne F V Chevance, Kelly T Hughes
Aug 30, 2008·Current Biology : CB·Howard C Berg
Nov 21, 2008·Proceedings of the National Academy of Sciences of the United States of America·Steven L PorterJudith P Armitage
Jul 3, 2009·Proceedings of the National Academy of Sciences of the United States of America·Teuta PilizotaJudith P Armitage
Jan 19, 2010·Current Opinion in Microbiology·Rong Gao, Ann M Stock
Mar 10, 2010·Current Opinion in Microbiology·Robert B Bourret
May 5, 2010·Proceedings of the National Academy of Sciences of the United States of America·Mayukh K SarkarDavid Blair
May 7, 2010·Molecular Microbiology·Xin Fang, Mark Gomelsky
Sep 3, 2010·PLoS Computational Biology·Marcus J TindallJudith P Armitage
Nov 20, 2010·Environmental Microbiology·Tino KrellJuan Luis Ramos
Jan 6, 2011·Proceedings of the National Academy of Sciences of the United States of America·Li XieXiao-Lun Wu

❮ Previous
Next ❯

Citations

Mar 10, 2018·Angewandte Chemie·Carlotta FolettiHelma Wennemers
May 11, 2019·PLoS Genetics·Leila M Reyes RuizSean Crosson
May 19, 2019·Annual Review of Microbiology·Rong GaoAnn M Stock
Nov 20, 2019·Journal of Bacteriology·Michael Y Galperin, Shan-Ho Chou
Nov 27, 2019·FEMS Microbiology Reviews·Tom E P Kimkes, Matthias Heinemann
Apr 25, 2020·Environmental Microbiology·Guang-Lei MaZhao-Xun Liang
Sep 10, 2020·Annual Review of Microbiology·Benoît-Joseph Laventie, Urs Jenal
Jan 22, 2020·Nature Reviews. Microbiology·Yves F Dufrêne, Alexandre Persat
Feb 6, 2020·Frontiers in Microbiology·Alejandra AlvaradoChristine Josenhans
Mar 10, 2020·FEMS Microbiology Reviews·Morgan BeebyDavid R Mitchell
Jul 3, 2020·Proceedings of the National Academy of Sciences of the United States of America·Chee-Seng HeeStephan Grzesiek
Feb 11, 2021·Science Advances·Wiem AbidiPetya Violinova Krasteva
Mar 17, 2020·Current Opinion in Microbiology·Catriona Ma Thompson, Jacob G Malone
Mar 1, 2021·Current Opinion in Microbiology·David M Hershey
Sep 7, 2020·Biophysical Journal·Paige WheatleyShahid Khan
Jun 5, 2021·Communications Biology·Marianne Grognot, Katja M Taute
Jul 21, 2021·Infection, Genetics and Evolution : Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases·Xiaoyan WanGuanghai Ji

❮ Previous
Next ❯

Datasets Mentioned

BETA
AB1770

Methods Mentioned

BETA
isothermal titration calorimetry
NMR
light scattering
microscale thermophoresis
two-hybrid
co-immunoprecipitation
fluorescence microscopy
size exclusion chromatography
electrophoresis
X-ray

Software Mentioned

ProtParam
Jackhmmer
ImageJ
ASTRA
Blast
Geneious Pro
PhyloPhlAn
PSI
MAFFT
GraphPad

Related Concepts

Trending Feeds

COVID-19

Coronaviruses encompass a large family of viruses that cause the common cold as well as more serious diseases, such as the ongoing outbreak of coronavirus disease 2019 (COVID-19; formally known as 2019-nCoV). Coronaviruses can spread from animals to humans; symptoms include fever, cough, shortness of breath, and breathing difficulties; in more severe cases, infection can lead to death. This feed covers recent research on COVID-19.

Blastomycosis

Blastomycosis fungal infections spread through inhaling Blastomyces dermatitidis spores. Discover the latest research on blastomycosis fungal infections here.

Nuclear Pore Complex in ALS/FTD

Alterations in nucleocytoplasmic transport, controlled by the nuclear pore complex, may be involved in the pathomechanism underlying multiple neurodegenerative diseases including Amyotrophic Lateral Sclerosis and Frontotemporal Dementia. Here is the latest research on the nuclear pore complex in ALS and FTD.

Applications of Molecular Barcoding

The concept of molecular barcoding is that each original DNA or RNA molecule is attached to a unique sequence barcode. Sequence reads having different barcodes represent different original molecules, while sequence reads having the same barcode are results of PCR duplication from one original molecule. Discover the latest research on molecular barcoding here.

Chronic Fatigue Syndrome

Chronic fatigue syndrome is a disease characterized by unexplained disabling fatigue; the pathology of which is incompletely understood. Discover the latest research on chronic fatigue syndrome here.

Evolution of Pluripotency

Pluripotency refers to the ability of a cell to develop into three primary germ cell layers of the embryo. This feed focuses on the mechanisms that underlie the evolution of pluripotency. Here is the latest research.

Position Effect Variegation

Position Effect Variagation occurs when a gene is inactivated due to its positioning near heterochromatic regions within a chromosome. Discover the latest research on Position Effect Variagation here.

STING Receptor Agonists

Stimulator of IFN genes (STING) are a group of transmembrane proteins that are involved in the induction of type I interferon that is important in the innate immune response. The stimulation of STING has been an active area of research in the treatment of cancer and infectious diseases. Here is the latest research on STING receptor agonists.

Microbicide

Microbicides are products that can be applied to vaginal or rectal mucosal surfaces with the goal of preventing, or at least significantly reducing, the transmission of sexually transmitted infections. Here is the latest research on microbicides.