A divergent CheW confers plasticity to nucleoid-associated chemosensory arrays

English version

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
doi: 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:

Cell fusion – Cell motility – Crystal structure – Fluorescence microscopy – Histidine – Phosphorylation – Protein structure – 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