A divergent CheW confers plasticity to nucleoid-associated chemosensory arrays
Autoři:
Annick Guiseppi aff001; Juan Jesus Vicente aff002; Julien Herrou aff001; Deborah Byrne aff003; Aurelie Barneoud aff001; Audrey Moine aff001; Leon Espinosa aff001; Marie-Jeanne Basse aff004; Virginie Molle aff005; Tâm Mignot aff001; Philippe Roche aff004; Emilia M. F. Mauriello aff001
Působiště autorů:
Laboratoire de Chimie Bactérienne, Aix Marseille Univ, CNRS, Marseille, France
aff001; Physiology & Biophysics, University of Washington, Seattle, WA, United States of America
aff002; Protein Purification Platform, Institut de Microbiologie de la Méditerranée, CNRS, Marseille, France
aff003; CRCM, Institute Paoli-Calmettes, CNRS, INSERM, Aix Marseille Univ, Marseille, France
aff004; Laboratoire de Dynamique des Interactions Membranaires Normales et Pathologique, Montpellier II et I University, CNRS, France
aff005
Vyšlo v časopise:
A divergent CheW confers plasticity to nucleoid-associated chemosensory arrays. PLoS Genet 15(12): e32767. doi:10.1371/journal.pgen.1008533
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1008533
Souhrn
Chemosensory systems are highly organized signaling pathways that allow bacteria to adapt to environmental changes. The Frz chemosensory system from M. xanthus possesses two CheW-like proteins, FrzA (the core CheW) and FrzB. We found that FrzB does not interact with FrzE (the cognate CheA) as it lacks the amino acid region responsible for this interaction. FrzB, instead, acts upstream of FrzCD in the regulation of M. xanthus chemotaxis behaviors and activates the Frz pathway by allowing the formation and distribution of multiple chemosensory clusters on the nucleoid. These results, together, show that the lack of the CheA-interacting region in FrzB confers new functions to this small protein.
Klíčová slova:
Crystal structure – Cell motility – Fluorescence microscopy – Histidine – Protein structure – Phosphorylation – Cell fusion – Protein structure comparison
Zdroje
1. Sourjik V, Berg HC. Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer. Proc Natl Acad Sci U S A. 2002;99: 12669–12674. doi: 10.1073/pnas.192463199 12232047
2. Berleman JE, Bauer CE. Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol Microbiol. 2005;56: 1457–1466. doi: 10.1111/j.1365-2958.2005.04646.x 15916598
3. Bible A, Russell MH, Alexandre G. The Azospirillum brasilense Che1 chemotaxis pathway controls swimming velocity, which affects transient cell-to-cell clumping. J Bacteriol. 2012;194: 3343–3355. doi: 10.1128/JB.00310-12 22522896
4. Collins KD, Lacal J, Ottemann KM. Internal sense of direction: sensing and signaling from cytoplasmic chemoreceptors. Microbiol Mol Biol Rev MMBR. 2014;78: 672–684. doi: 10.1128/MMBR.00033-14 25428939
5. Bilwes AM, Alex LA, Crane BR, Simon MI. Structure of CheA, a signal-transducing histidine kinase. Cell. 1999;96: 131–141. doi: 10.1016/s0092-8674(00)80966-6 9989504
6. Griswold IJ, Zhou H, Matison M, Swanson RV, McIntosh LP, Simon MI, et al. The solution structure and interactions of CheW from Thermotoga maritima. Nat Struct Biol. 2002;9: 121–125. doi: 10.1038/nsb753 11799399
7. Reebye V, Frilling A, Hajitou A, Nicholls JP, Habib NA, Mintz PJ. A perspective on non-catalytic Src homology (SH) adaptor signalling proteins. Cell Signal. 2012;24: 388–392. doi: 10.1016/j.cellsig.2011.10.003 22024281
8. Li X, Fleetwood AD, Bayas C, Bilwes AM, Ortega DR, Falke JJ, et al. The 3.2 Å resolution structure of a receptor: CheA:CheW signaling complex defines overlapping binding sites and key residue interactions within bacterial chemosensory arrays. Biochemistry. 2013;52: 3852–3865. doi: 10.1021/bi400383e 23668907
9. Khursigara CM, Wu X, Subramaniam S. Chemoreceptors in Caulobacter crescentus: trimers of receptor dimers in a partially ordered hexagonally packed array. J Bacteriol. 2008;190: 6805–6810. doi: 10.1128/JB.00640-08 18689468
10. Briegel A, Ortega DR, Tocheva EI, Wuichet K, Li Z, Chen S, et al. Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci U S A. 2009;106: 17181–17186. doi: 10.1073/pnas.0905181106 19805102
11. Briegel A, Li X, Bilwes AM, Hughes KT, Jensen GJ, Crane BR. Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proc Natl Acad Sci U S A. 2012;109: 3766–3771. doi: 10.1073/pnas.1115719109 22355139
12. Sourjik V, Berg HC. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol. 2000;37: 740–751. doi: 10.1046/j.1365-2958.2000.02044.x 10972797
13. Wadhams GH, Martin AC, Warren AV, Armitage JP. Requirements for chemotaxis protein localization in Rhodobacter sphaeroides. Mol Microbiol. 2005;58: 895–902. doi: 10.1111/j.1365-2958.2005.04880.x 16238635
14. Sourjik V, Berg HC. Functional interactions between receptors in bacterial chemotaxis. Nature. 2004;428: 437–441. doi: 10.1038/nature02406 15042093
15. Ames P, Parkinson JS. Conformational suppression of inter-receptor signaling defects. Proc Natl Acad Sci U S A. 2006;103: 9292–9297. doi: 10.1073/pnas.0602135103 16751275
16. Li M, Hazelbauer GL. Selective allosteric coupling in core chemotaxis signaling complexes. Proc Natl Acad Sci U S A. 2014;111: 15940–15945. doi: 10.1073/pnas.1415184111 25349385
17. Piñas GE, Frank V, Vaknin A, Parkinson JS. The source of high signal cooperativity in bacterial chemosensory arrays. Proc Natl Acad Sci U S A. 2016;113: 3335–3340. doi: 10.1073/pnas.1600216113 26951681
18. Blackhart BD, Zusman DR. “Frizzy” genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility. Proc Natl Acad Sci U S A. 1985;82: 8767–8770. doi: 10.1073/pnas.82.24.8767 3936045
19. Treuner-Lange A, Macia E, Guzzo M, Hot E, Faure LM, Jakobczak B, et al. The small G-protein MglA connects to the MreB actin cytoskeleton at bacterial focal adhesions. J Cell Biol. 2015;210: 243–256. doi: 10.1083/jcb.201412047 26169353
20. Guzzo M, Agrebi R, Espinosa L, Baronian G, Molle V, Mauriello EMF, et al. Evolution and Design Governing Signal Precision and Amplification in a Bacterial Chemosensory Pathway. PLoS Genet. 2015;11: e1005460. doi: 10.1371/journal.pgen.1005460 26291327
21. Chang Y-W, Rettberg LA, Treuner-Lange A, Iwasa J, Søgaard-Andersen L, Jensen GJ. Architecture of the type IVa pilus machine. Science. 2016;351: aad2001. doi: 10.1126/science.aad2001 26965631
22. Bustamante VH, Martinez-Flores I, Vlamakis HC, Zusman DR. Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol Microbiol. 2004;53: 1501–13. doi: 10.1111/j.1365-2958.2004.04221.x 15387825
23. Mauriello EMF, Jones C, Moine A, Armitage JP. Cellular targeting and segregation of bacterial chemosensory systems. FEMS Microbiol Rev. 2018;42: 462–476. doi: 10.1093/femsre/fuy015 29945173
24. McBride MJ, Weinberg RA, Zusman DR. “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria. Proc Natl Acad Sci U S A. 1989;86: 424–428. doi: 10.1073/pnas.86.2.424 2492105
25. Concepcion J, Witte K, Wartchow C, Choo S, Yao D, Persson H, et al. Label-free detection of biomolecular interactions using BioLayer interferometry for kinetic characterization. Comb Chem High Throughput Screen. 2009;12: 791–800. doi: 10.2174/138620709789104915 19758119
26. Inclán YF, Vlamakis HC, Zusman DR. FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus. Mol Microbiol. 2007;65: 90–102. doi: 10.1111/j.1365-2958.2007.05774.x 17581122
27. Kaimer C, Zusman DR. Regulation of cell reversal frequency in Myxococcus xanthus requires the balanced activity of CheY-like domains in FrzE and FrzZ. Mol Microbiol. 2016;100: 379–395. doi: 10.1111/mmi.13323 26748740
28. Moine A, Espinosa L, Martineau E, Yaikhomba M, Jazleena PJ, Byrne D, et al. The nucleoid as a scaffold for the assembly of bacterial signaling complexes. PLOS Genet. 2017;13: e1007103. doi: 10.1371/journal.pgen.1007103 29161263
29. Liu J, Hu B, Morado DR, Jani S, Manson MD, Margolin W. Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. Proc Natl Acad Sci U S A. 2012;109: E1481–1488. doi: 10.1073/pnas.1200781109 22556268
30. Cassidy CK, Himes BA, Alvarez FJ, Ma J, Zhao G, Perilla JR, et al. CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling. eLife. 2015;4. doi: 10.7554/eLife.08419 26583751
31. Moine A, Agrebi R, Espinosa L, Kirby JR, Zusman DR, Mignot T, et al. Functional organization of a multimodular bacterial chemosensory apparatus. PLoS Genet. 2014;10: e1004164. doi: 10.1371/journal.pgen.1004164 24603697
32. Adams DW, Wu LJ, Errington J. Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J. 2015;34: 491–501. doi: 10.15252/embj.201490177 25568309
33. McBride MJ, Köhler T, Zusman DR. Methylation of FrzCD, a methyl-accepting taxis protein of Myxococcus xanthus, is correlated with factors affecting cell behavior. J Bacteriol. 1992;174: 4246–4257. doi: 10.1128/jb.174.13.4246-4257.1992 1624419
34. Mauriello EMF, Nan B, Zusman DR. AglZ regulates adventurous (A-) motility in Myxococcus xanthus through its interaction with the cytoplasmic receptor, FrzCD. Mol Microbiol. 2009;72: 964–977. doi: 10.1111/j.1365-2958.2009.06697.x 19400788
35. Nan B, Mauriello EMF, Sun I-H, Wong A, Zusman DR. A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol Microbiol. 2010;76: 1539–1554. doi: 10.1111/j.1365-2958.2010.07184.x 20487265
36. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 2008;36: W197–W201. doi: 10.1093/nar/gkn238 18463136
37. Sievers F, Higgins DG. Clustal omega. Curr Protoc Bioinforma Ed Board Andreas Baxevanis Al. 2014;48: 3.13.1–16. doi: 10.1002/0471250953.bi0313s48 25501942
38. Webb B, Sali A. Comparative Protein Structure Modeling Using MODELLER. Curr Protoc Bioinforma Ed Board Andreas Baxevanis Al. 2016;54: 5.6.1–5.6.37. doi: 10.1002/cpbi.3 27322406
39. Park S-Y, Borbat PP, Gonzalez-Bonet G, Bhatnagar J, Pollard AM, Freed JH, et al. Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol. 2006;13: 400–407. doi: 10.1038/nsmb1085 16622408
40. Krissinel E, Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr. 2004;60: 2256–2268. doi: 10.1107/S0907444904026460 15572779
41. Gouet P, Robert X, Courcelle E. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 2003;31: 3320–3323. doi: 10.1093/nar/gkg556 12824317
42. Mignot T, Merlie JP, Zusman DR. Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science. 2005;310: 855–7. doi: 10.1126/science.1119052 16272122
43. Ducret A, Maisonneuve E, Notareschi P, Grossi A, Mignot T, Dukan S. A microscope automated fluidic system to study bacterial processes in real time. PloS One. 2009;4: e7282. doi: 10.1371/journal.pone.0007282 19789641
44. Ducret A, Quardokus EM, Brun YV. MicrobeJ, a tool for high throughput bacterial cell detection and quantitative analysis. Nat Microbiol. 2016;1: 16077. doi: 10.1038/nmicrobiol.2016.77 27572972
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2019 Číslo 12
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Aspergillus fumigatus calcium-responsive transcription factors regulate cell wall architecture promoting stress tolerance, virulence and caspofungin resistance
- Architecture of the Escherichia coli nucleoid
- Common gardens in teosintes reveal the establishment of a syndrome of adaptation to altitude
- Restricted and non-essential redundancy of RNAi and piRNA pathways in mouse oocytes