Polar Flagellar Biosynthesis and a Regulator of Flagellar Number Influence Spatial Parameters of Cell Division in

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Spatial and numerical regulation of flagellar biosynthesis results in different flagellation patterns specific for each bacterial species. Campylobacter jejuni produces amphitrichous (bipolar) flagella to result in a single flagellum at both poles. These flagella confer swimming motility and a distinctive darting motility necessary for infection of humans to cause diarrheal disease and animals to promote commensalism. In addition to flagellation, symmetrical cell division is spatially regulated so that the divisome forms near the cellular midpoint. We have identified an unprecedented system for spatially regulating cell division in C. jejuni composed by FlhG, a regulator of flagellar number in polar flagellates, and components of amphitrichous flagella. Similar to its role in other polarly-flagellated bacteria, we found that FlhG regulates flagellar biosynthesis to limit poles of C. jejuni to one flagellum. Furthermore, we discovered that FlhG negatively influences the ability of FtsZ to initiate cell division. Through analysis of specific flagellar mutants, we discovered that components of the motor and switch complex of amphitrichous flagella are required with FlhG to specifically inhibit division at poles. Without FlhG or specific motor and switch complex proteins, cell division occurs more often at polar regions to form minicells. Our findings suggest a new understanding for the biological requirement of the amphitrichous flagellation pattern in bacteria that extend beyond motility, virulence, and colonization. We propose that amphitrichous bacteria such as Campylobacter species advantageously exploit placement of flagella at both poles to spatially regulate an FlhG-dependent mechanism to inhibit polar cell division, thereby encouraging symmetrical cell division to generate the greatest number of viable offspring. Furthermore, we found that other polarly-flagellated bacteria produce FlhG proteins that influence cell division, suggesting that FlhG and polar flagella may function together in a broad range of bacteria to spatially regulate division.

Vyšlo v časopise: Polar Flagellar Biosynthesis and a Regulator of Flagellar Number Influence Spatial Parameters of Cell Division in. PLoS Pathog 7(12): e32767. doi:10.1371/journal.ppat.1002420
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002420

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1. CorreaNEPengFKloseKE 2005 Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription heirarchy. J Bacteriol 187 6324 6332

2. DasguptaNAroraSKRamphalR 2000 fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 182 357 364

3. KusumotoAKamisakaKYakushiTTerashimaHShinoharaA 2006 Regulation of polar flagellar number by the flhF and flhG genes in Vibrio alginolyticus. J Biochem 139 113 121

4. KusumotoAShinoharaATerashimaHKojimaSYakushiT 2008 Collaboration of FlhF and FlhG to regulate polar-flagella number and localization in Vibrio alginolyticus. Microbiology 154 1390 1399

5. GreenJCKahramanoglouCRahmanAPenderAMCharbonnelN 2009 Recruitment of the earliest component of the bacterial flagellum to the old cell division pole by a membrane-associated signal recognition particle family GTP-binding protein. J Mol Biol 391 679 690

6. BalabanMJoslinSNHendrixsonDR 2009 FlhF and its GTPase activity are required for distinct processes in flagellar gene regulation and biosynthesis in Campylobacter jejuni. J Bacteriol 191 6602 6611

7. MurrayTSKazmierczakBI 2006 FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J Bacteriol 188 6995 7004

8. BarakIWilkinsonAJ 2007 Division site recognition in Escherichia coli and Bacillus subtilis. FEMS Microbiol Rev 31 311 326

9. LutkenhausJ 2007 Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76 539 562

10. de BoerPACrossleyREHandARRothfieldLI 1991 The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. Embo J 10 4371 4380

11. KarouiMEErringtonJ 2001 Isolation and characterization of topological specificity mutants of minD in Bacillus subtilis. Mol Microbiol 42 1211 1221

12. BiELutkenhausJ 1993 Cell division inhibitors SulA and MinCD prevent formation of the FtsZ ring. J Bacteriol 175 1118 1125

13. de BoerPACrossleyRERothfieldLI 1992 Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol 174 63 70

14. HuZMukherjeeAPichoffSLutkenhausJ 1999 The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci U S A 96 14819 14824

15. MarstonALErringtonJ 1999 Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol 33 84 96

16. de BoerPACrossleyRERothfieldLI 1989 A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56 641 649

17. ChaJHStewartGC 1997 The divIVA minicell locus of Bacillus subtilis. J Bacteriol 179 1671 1683

18. HuZLutkenhausJ 2001 Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 7 1337 1343

19. HuZGogolEPLutkenhausJ 2002 Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci U S A 99 6761 6766

20. LacknerLLRaskinDMde BoerPA 2003 ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 185 735 749

21. FuXShihYLZhangYRothfieldLI 2001 The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc Natl Acad Sci U S A 98 980 985

22. HaleCAMeinhardtHde BoerPA 2001 Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. Embo J 20 1563 1572

23. RaskinDMde BoerPA 1999 Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci U S A 96 4971 4976

24. RaskinDMde BoerPA 1999 MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181 6419 6424

25. RaskinDMde BoerPA 1997 The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli. Cell 91 685 694

26. MarstonALThomaidesHBEdwardsDHSharpeMEErringtonJ 1998 Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev 12 3419 3430

27. PatrickJEKearnsDB 2008 MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol 70 1166 1179

28. BramkampMEmminsRWestonLDonovanCDanielRA 2008 A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol Microbiol 70 1556 1569

29. GregoryJABeckerECPoglianoK 2008 Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes Dev 22 3475 3488

30. WoldringhCLMulderEValkenburgJAWientjesFBZaritskyA 1990 Role of the nucleoid in the toporegulation of division. Res Microbiol 141 39 49

31. SunQYuXCMargolinW 1998 Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol Microbiol 29 491 503

32. YuXCMargolinW 1999 FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol Microbiol 32 315 326

33. WuLJErringtonJ 2004 Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117 915 925

34. BernhardtTGde BoerPA 2005 SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18 555 564

35. ChoHMcManusHRDoveSLBernhardtTG 2011 Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci U S A 108 3773 3778

36. ThanbichlerMShapiroL 2006 MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126 147 162

37. BlackRELevineMMClementsMLHughesTPBlaserMJ 1988 Experimental Campylobacter jejuni infection in humans. J Infect Dis 157 472 479

38. NachamkinIYangX-HSternNJ 1993 Role of Campylobacter jejuni flagella as colonization factors for three-day-old chicks: analysis with flagellar mutants. Appl Environ Microbiol 59 1269 1273

39. HendrixsonDRDiRitaVJ 2004 Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol Microbiol 52 471 484

40. WassenaarTMvan der ZeijstBAMAylingRNewellDG 1993 Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139 Pt6 1171 1175

41. DasguptaNRamphalR 2001 Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 183 6636 6644

42. VarleyAWStewartGC 1992 The divIVB region of the Bacillus subtilis chromosome encodes homologs of Escherichia coli septum placement (minCD) and cell shape (mreBCD) determinants. J Bacteriol 174 6729 6742

43. TeatherRMCollinsJFDonachieWD 1974 Quantal behavior of a diffusible factor which initiates septum formation at potential division sites in Escherichia coli. J Bacteriol 118 407 413

44. JaffeAD'AriRHiragaS 1988 Minicell-forming mutants of Escherichia coli: production of minicells and anucleate rods. J Bacteriol 170 3094 3101

45. BottaGAParkJT 1981 Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation. J Bacteriol 145 333 340

46. SprattBGPardeeAB 1975 Penicillin-binding proteins and cell shape in E. coli. Nature 254 516 517

47. HayashiIOyamaTMorikawaK 2001 Structural and functional studies of MinD ATPase: implications for the molecular recognition of the bacterial cell division apparatus. Embo J 20 1819 1828

48. LeonardTAButlerPJLoweJ 2005 Bacterial chromosome segregation: structure and DNA binding of the Soj dimer--a conserved biological switch. Embo J 24 270 282

49. WuWParkKTHolyoakTLutkenhausJ 2011 Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol Microbiol 79 1515 28

50. WardJEJrLutkenhausJ 1985 Overproduction of FtsZ induces minicell formation in E. coli. Cell 42 941 949

51. ParrishJRYuJLiuGHinesJAChanJE 2007 A proteome-wide protein interaction map for Campylobacter jejuni. Genome Biol 8 R130

52. PandzaSBaetensMParkCHAuTKeyhanM 2000 The G-protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida. Mol Microbiol 36 414 423

53. EwingCPAndreishchevaEGuerryP 2009 Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J Bacteriol 191 7086 7093

54. HendrixsonDRDiRitaVJ 2003 Transcription of σ54-dependent but not σ28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol Microbiol 50 687 702

55. MacnabRM 2003 How bacteria assemble flagella. Annu Rev Microbiol 57 77 100

56. HuZLutkenhausJ 1999 Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor MinC under the control of MinD and MinE. Mol Microbiol 34 82 90

57. SzetoTHRowlandSLRothfieldLIKingGF 2002 Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci U S A 99 15693 15698

58. HuZLutkenhausJ 2003 A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 47 345 355

59. SzetoTHRowlandSLHabrukowichCLKingGF 2003 The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 278 40050 40056

60. ZhouHSchulzeRCoxSSaezCHuZ 2005 Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol 187 629 638

61. de BoerPCrossleyRRothfieldL 1992 The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359 254 256

62. RayChaudhuriDParkJT 1992 Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359 251 254

63. MukherjeeALutkenhausJ 1998 Dynamic assembly of FtsZ regulated by GTP hydrolysis. Embo J 17 462 469

64. ShigematsuMUmedaAFujimotoSAmakoK 1998 Spirochaete-like swimming mode of Campylobacter jejuni in a viscous environment. J Med Microbiol 47 521 526

65. SzymanskiCMKingMHaardtMArmstrongGD 1995 Campylobacter jejuni motility and invasion of Caco-2 cells. Infect Immun 63 4295 4300

66. BaconDJAlmRABurrDHHuLKopeckoDJ 2000 Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 68 4384 4390

67. FigurskiDHHelinskiDR 1979 Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76 1648 1652

68. GuerryPYaoRAlmRABurrDHTrustTJ 1994 Systems of experimental genetics for Campylobacter species. Methods Enzymol 235 474 481