ATPase-Independent Type-III Protein Secretion in

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The type-III protein secretion apparatus is a complex nanomachine responsible for secretion of building blocks and substrate proteins of the flagellum and the virulence-associated injectisome needle complex of many gram-negative pathogens. Type-III secretion systems utilize the energy of the proton motive force and ATP hydrolysis of a cytoplasmic ATPase to drive substrate export. The cytoplasmic components of the secretion system share strong homology to the FoF1 ATP synthase and it is thought that the flagellum was derived from a proto FoF1-ATP synthase where ATP hydrolysis energized the export process. Here, we report the dispensability of ATPase activity for the type-III protein export process in Salmonella. This finding has important implications for the evolution of the bacterial flagellum and type-III secretion systems, suggesting that a proto ATPase was added to a primordial proton-powered type-III export system with the evolutionary benefit of facilitating the export process.

Vyšlo v časopise: ATPase-Independent Type-III Protein Secretion in. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004800
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004800

Souhrn

Zdroje

1. BergHC, AndersonRA (1973) Bacteria swim by rotating their flagellar filaments. Nature 245: 380–382.

2. ChevanceFFV, HughesKT (2008) Coordinating assembly of a bacterial macromolecular machine. Nature Reviews Microbiology 6: 455–465.

3. KearnsDB (2010) A field guide to bacterial swarming motility. Nature Reviews Microbiology 8: 634–644.

4. DuanQ, ZhouM, ZhuL, ZhuG (2013) Flagella and bacterial pathogenicity. Journal of Basic Microbiology 53: 1–8..

5. CornelisGR (2006) The type III secretion injectisome. Nature Reviews Microbiology 4: 811–825.

6. MacnabRM (2004) Type III flagellar protein export and flagellar assembly. Biochimica et Biophysica Acta 1694: 207–217.

7. ThomasDR, FrancisNR, XuC, DeRosierDJ (2006) The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. Journal of Bacteriology 188: 7039–7048.

8. FanF, OhnishiK, FrancisNR, MacnabRM (1997) The FliP and FliR proteins of Salmonella typhimurium, putative components of the type III flagellar export apparatus, are located in the flagellar basal body. Molecular Microbiology 26: 1035–1046.

9. ClaretL, CalderSR, HigginsM, HughesC (2003) Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Molecular Microbiology 48: 1349–1355.

10. MinaminoT, MacnabRM (2000) FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity. Molecular Microbiology 37: 1494–1503.

11. Gonzalez-PedrajoB, FraserGM, MinaminoT, MacnabRM (2002) Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway. Molecular Microbiology 45: 967–982.

12. IbukiT, ImadaK, MinaminoT, KatoT, MiyataT, et al. (2011) Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nature Structural & Molecular Biology 18: 277–282.

13. ImadaK, MinaminoT, TaharaA, NambaK (2007) Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proceedings of the National Academy of Sciences of the United States of America 104: 485–490.

14. PallenMJ, BaileyCM, BeatsonSA (2006) Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases. Protein Sci 15: 935–941.

15. PaulK, ErhardtM, HiranoT, BlairDF, HughesKT (2008) Energy source of flagellar type III secretion. Nature 451: 489–492.

16. MinaminoT, NambaK (2008) Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451: 485.

17. AkedaY, GalanJE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911–915.

18. González-PedrajoB, MinaminoT, KiharaM, NambaK (2006) Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Molecular Microbiology 60: 984–998.

19. McMurryJL, MurphyJW, González-PedrajoB (2006) The FliN-FliH interaction mediates localization of flagellar export ATPase FliI to the C ring complex. Biochemistry 45: 11790–11798.

20. BangeG, KümmererN, EngelC, BozkurtG, WildK, et al. (2010) FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proceedings of the National Academy of Sciences of the United States of America 107: 11295–300.

21. MinaminoT, MorimotoYV, HaraN, NambaK (2011) An energy transduction mechanism used in bacterial flagellar type III protein export. Nature communications 2: 475.

22. MinaminoT, ChuR, YamaguchiS, MacnabRM (2000) Role of FliJ in flagellar protein export in Salmonella. Journal of Bacteriology 182: 4207–4215.

23. EvansLDB, StaffordGP, AhmedS, FraserGM, HughesC (2006) An escort mechanism for cycling of export chaperones during flagellum assembly. Proceedings of the National Academy of Sciences of the United States of America 103: 17474–17479.

24. KuboriT, MatsushimaY, NakamuraD, UralilJ, Lara-TejeroM, et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science (New York, NY) 280: 602–605.

25. EichelbergK, GinocchioCC, GalanJE (1994) Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins. Journal of Bacteriology 176: 4501–4510.

26. MinaminoT, Gonzalez-PedrajoB, KiharaM, NambaK, MacnabRM (2003) The ATPase FliI can interact with the type III flagellar protein export apparatus in the absence of its regulator, FliH. Journal of Bacteriology 185: 3983–3988.

27. TomoyasuT, TakayaA, IsogaiE, YamamotoT (2003) Turnover of FlhD and FlhC, master regulator proteins for Salmonella flagellum biogenesis, by the ATP-dependent ClpXP protease. Molecular Microbiology 48: 443–452.

28. ErhardtM, HughesKT (2010) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Molecular Microbiology 75: 376–393.

29. JensenPR, MichelsenO (1992) Carbon and energy metabolism of atp mutants of Escherichia coli. Journal of Bacteriology 174: 7635–7641.

30. Koch-KoerfgesA, KabusA, OchrombelI, MarinK, BottM (2012) Physiology and global gene expression of a Corynebacterium glutamicum ΔF(1)F(O)-ATP synthase mutant devoid of oxidative phosphorylation. Biochimica et Biophysica Acta 1817: 370–380.

31. Martinez-ArgudoI, VeenendaalAKJ, LiuX, RoehrichAD, RonessenMC, et al. (2013) Isolation of Salmonella mutants resistant to the inhibitory effect of Salicylidene acylhydrazides on flagella-mediated motility. PLoS ONE 8: e52179.

32. ErhardtM, SingerHM, WeeDH, KeenerJP, HughesKT (2011) An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. The EMBO Journal 30: 2948–2961.

33. HaraN, NambaK, MinaminoT (2011) Genetic Characterization of Conserved Charged Residues in the Bacterial Flagellar Type III Export Protein FlhA. PLoS ONE 6: e22417.

34. Galán JE (2008) Energizing type III secretion machines: what is the fuel? Nature Structural & Molecular Biology. pp. 127–128.

35. LeeHJ, HughesKT (2006) Posttranscriptional control of the Salmonella enterica flagellar hook protein FlgE. Journal of Bacteriology 188: 3308–3316.

36. GalanJE (2001) Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 17: 53–86.

37. AkedaY, GalanJE (2004) Genetic analysis of the Salmonella enterica type III secretion-associated ATPase InvC defines discrete functional domains. Journal of Bacteriology 186: 2402–2412.

38. KuboriT, ShimamotoN, YamaguchiS, NambaK, AizawaS (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. Journal of Molecular Biology 226: 433–446.

39. MorimotoYV, ItoM, HiraokaKD, CheYS, BaiF, et al. (2014) Assembly and stoichiometry of FliF and FlhA in Salmonella flagellar basal body. Mol Microbiol 91: 1214–1226.

40. BertaniG (2004) Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. Journal of Bacteriology 186: 595–600.

41. SandersonKE, RothJR (1983) Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev 47: 410–453.

42. SingerHM, ErhardtM, SteinerAM, ZhangM-M, YoshikamiD, et al. (2012) Selective purification of recombinant neuroactive peptides using the flagellar type III secretion system. mBio 3.

43. BajajV, LucasRL, HwangC, LeeCA (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Molecular Microbiology 22: 703–714.

44. AbramoffM, MagelhaesPJ, RamSJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36–42.

45. SbalzariniIF, KoumoutsakosP (2005) Feature point tracking and trajectory analysis for video imaging in cell biology. J Struct Biol 151: 182–195.

46. BoehmA, KaiserM, LiH, SpanglerC, KasperCA, et al. (2010) Second Messenger-Mediated Adjustment of Bacterial Swimming Velocity. Cell 141: 107–116.

47. BonifieldHR, HughesKT (2003) Flagellar phase variation in Salmonella enterica is mediated by a posttranscriptional control mechanism. Journal of Bacteriology 185: 3567–3574.