#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Modulation of flagellar rotation in surface-attached bacteria: A pathway for rapid surface-sensing after flagellar attachment


Autoři: Maren Schniederberend aff001;  Jessica F. Williams aff002;  Emilee Shine aff003;  Cong Shen aff003;  Ruchi Jain aff001;  Thierry Emonet aff002;  Barbara I. Kazmierczak aff001
Působiště autorů: Department of Medicine (Infectious Diseases), Yale University, New Haven, Connecticut, United States of America aff001;  Department of Molecular, Cellular & Developmental Biology, Yale University, New Haven, Connecticut, United States of America aff002;  Program in Microbiology, Yale University, New Haven, Connecticut, United States of America aff003;  Department of Physics, Yale University, New Haven, Connecticut, United States of America aff004;  Department of Microbial Pathogenesis, Yale University, New Haven, Connecticut, United States of America aff005
Vyšlo v časopise: Modulation of flagellar rotation in surface-attached bacteria: A pathway for rapid surface-sensing after flagellar attachment. PLoS Pathog 15(11): e32767. doi:10.1371/journal.ppat.1008149
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008149

Souhrn

Attachment is a necessary first step in bacterial commitment to surface-associated behaviors that include colonization, biofilm formation, and host-directed virulence. The Gram-negative opportunistic pathogen Pseudomonas aeruginosa can initially attach to surfaces via its single polar flagellum. Although many bacteria quickly detach, some become irreversibly attached and express surface-associated structures, such as Type IV pili, and behaviors, including twitching motility and biofilm initiation. P. aeruginosa that lack the GTPase FlhF assemble a randomly placed flagellum that is motile; however, we observed that these mutant bacteria show defects in biofilm formation comparable to those seen for non-motile, aflagellate bacteria. This phenotype was associated with altered behavior of ΔflhF bacteria immediately following surface-attachment. Forward and reverse genetic screens led to the discovery that FlhF interacts with FimV to control flagellar rotation at a surface, and implicated cAMP signaling in this pathway. Although cAMP controls many transcriptional programs in P. aeruginosa, known targets of this second messenger were not required to modulate flagellar rotation in surface-attached bacteria. Instead, alterations in switching behavior of the motor appeared to result from direct or indirect effects of cAMP on switch complex proteins and/or the stators associated with them.

Klíčová slova:

Bacterial biofilms – Flagella – Intracellular pathogens – Pathogen motility – Pseudomonas aeruginosa – Swimming – Flagellar rotation – Adenylyl cyclase


Zdroje

1. O'Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol. 1998;30:295–304. doi: 10.1046/j.1365-2958.1998.01062.x 9791175

2. Conrad JC, Gibiansky ML, Jin F, Gordon VD, Motto DA, Mathewson MA, et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys J. 2011;100(7):1608–16. Epub 2011/04/06. doi: 10.1016/j.bpj.2011.02.020 21463573.

3. Caiazza NC, O'Toole GA. SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol. 2004;186:4476–85. doi: 10.1128/JB.186.14.4476-4485.2004 15231779

4. Lele PP, Hosu BG, Berg HC. Dynamics of mechanosensing in the bacterial flagellar motor. Proc Natl Acad Sci U S A. 2013;110:11839–44. doi: 10.1073/pnas.1305885110 23818629

5. Belas R, Simon M, Silverman M. Regulation of lateral flagella gene transcription in Vibrio parahaemolyticus. J Bacteriol. 1986;167:210–8. doi: 10.1128/jb.167.1.210-218.1986 3013835

6. McCarter L, Hilmen M, Silverman M. Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus. Cell. 1988;54:345–51. doi: 10.1016/0092-8674(88)90197-3 3396074

7. Belas R, Suvanasuthi R. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J Bacteriol. 2005;187(19):6789–803. doi: 10.1128/JB.187.19.6789-6803.2005 16166542.

8. Li G, Brown PJ, Tang JX, Xu J, Quardokus EM, Fuqua C, et al. Surface contact stimulates the just-in-time deployment of bacterial adhesins. Mol Microbiol. 2012;83(1):41–51. Epub 2011/11/08. doi: 10.1111/j.1365-2958.2011.07909.x 22053824.

9. Cairns LS, Marlow VL, Bissett E, Ostrowski A, Stanley-Wall NR. A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis. Mol Microbiol. 2013;90(1):6–21. Epub 2013/07/31. doi: 10.1111/mmi.12342 23888912.

10. Chawla R, Ford KM, Lele PP. Torque, but not FliL, regulates mechanosensitive flagellar motor-function. Scientific reports. 2017;7(1):5565. doi: 10.1038/s41598-017-05521-8 28717192.

11. Tipping MJ, Delalez NJ, Lim R, Berry RM, Armitage JP. Load-dependent assembly of the bacterial flagellar motor. mBio. 2013;4(4). Epub 2013/08/22. doi: 10.1128/mBio.00551-13 23963182.

12. Wadhwa N, Phillips R, Berg HC. Torque-dependent remodeling of the bacterial flagellar motor. Proc Natl Acad Sci U S A. 2019;116(24):11764–9. Epub 2019/05/31. doi: 10.1073/pnas.1904577116 31142644.

13. Belas R. Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 2014;22(9):517–27. Epub 2014/06/05. doi: 10.1016/j.tim.2014.05.002 24894628.

14. Hug I, Deshpande S, Sprecher KS, Pfohl T, Jenal U. Second messenger-mediated tactile response by a bacterial rotary motor. Science. 2017;358(6362):531–4. Epub 2017/10/28. doi: 10.1126/science.aan5353 29074777.

15. Laventie B-J, Sangermani M, Estermann F, Manfredi P, Planes R, Hug I, et al. A Surface-Induced Asymmetric Program Promotes Tissue Colonization by Pseudomonas aeruginosa. Cell Host & Microbe. 2019;25(1):140–52.e6. https://doi.org/10.1016/j.chom.2018.11.008.

16. Ellison CK, Kan J, Dillard RS, Kysela DT, Ducret A, Berne C, et al. Obstruction of pilus retraction stimulates bacterial surface sensing. Science. 2017;358(6362):535–8. Epub 2017/10/28. doi: 10.1126/science.aan5706 29074778.

17. Toutain CM, Caizza NC, Zegans ME, O'Toole GA. Roles for flagellar stators in biofilm formation by Pseudomonas aeruginosa. Res Microbiol. 2007;158(5):471–7. doi: 10.1016/j.resmic.2007.04.001 17533122.

18. Toutain CM, Zegans ME, O'Toole GA. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J Bacteriol. 2005;187:771–7. doi: 10.1128/JB.187.2.771-777.2005 15629949

19. Doyle TB, Hawkins AC, McCarter LL. The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol. 2004;186:6341–50. doi: 10.1128/JB.186.19.6341-6350.2004 15375113

20. Kuchma SL, Delalez NJ, Filkins LM, Snavely EA, Armitage JP, O'Toole GA. Cyclic di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa PA14 requires the MotAB stator. J Bacteriol. 2015;197(3):420–30. doi: 10.1128/JB.02130-14 25349157.

21. Baker AE, Diepold A, Kuchma SL, Scott JE, Ha DG, Orazi G, et al. PilZ Domain Protein FlgZ Mediates Cyclic Di-GMP-Dependent Swarming Motility Control in Pseudomonas aeruginosa. J Bacteriol. 2016;198(13):1837–46. doi: 10.1128/JB.00196-16 27114465.

22. Kazmierczak BI, Hendrixson DR. Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria. Mol Microbiol. 2013;88(4):655–63. Epub 2013/04/23. doi: 10.1111/mmi.12221 23600726.

23. Schniederberend M, Abdurachim K, Murray TS, Kazmierczak BI. The GTPase Activity of FlhF Is Dispensable for Flagellar Localization, but Not Motility, in Pseudomonas aeruginosa. J Bacteriol. 2013;195(5):1051–60. Epub 2012/12/25. doi: 10.1128/JB.02013-12 23264582.

24. Murray TS, Kazmierczak BI. FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J Bacteriol. 2006;188(19):6995–7004. doi: 10.1128/JB.00790-06 16980502

25. Gao T, Shi M, Ju L, Gao H. Investigation into FlhFG reveals distinct features of FlhF in regulating flagellum polarity in Shewanella oneidensis. Mol Microbiol. 2015;98:571–85. doi: 10.1111/mmi.13141 26194016

26. Correa NE, Peng F, Klose KE. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J Bacteriol. 2005;187:6324–32. doi: 10.1128/JB.187.18.6324-6332.2005 16159765

27. Balaban M, Joslin SN, Hendrixson DR. FlhF and its GTPase activity are required for distinct processes in flagellar gene regulation and biosynthesis in Campylobacter jejuni. J Bacteriol. 2009;191:6602–11. doi: 10.1128/JB.00884-09 19717591

28. Green JCD, Kahramanoglou C, Rahman A, Pender AMC, Charbonnel N, Fraser GM. 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. 2009;391:679–90. doi: 10.1016/j.jmb.2009.05.075 19497327

29. Kusumoto A, Nishioka N, Kojima S, Homma M. Mutational analysis of the GTP-binding motif of FlhF which regulates the number and placement of the polar flagellum in Vibrio alginolyticus. J Biochem. 2009;146(5):643–50. Epub 2009/07/17. doi: 10.1093/jb/mvp109 19605463.

30. Minamino T, Imada K. The bacterial flagellar motor and its structural diversity. Trends Microbiol. 2015;23(5):267–74. doi: 10.1016/j.tim.2014.12.011 25613993.

31. Coggan KA, Wolfgang MC. Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. Curr Issues Mol Biol. 2012;14:47–70. 22354680

32. Wolfgang MC, Lee VT, Gilmore ME, Lory S. Coordinate regulation of bacterial genes by a novel adenylate cyclase signaling pathway. Devlop Cell. 2003;4:253–63.

33. Serate J, Roberts GP, Berg O, Youn H. Ligand Responses of Vfr, the Virulence Factor Regulator from Pseudomonas aeruginosa. J Bacteriol. 2011;193(18):4859–68. Epub 2011/07/19. doi: 10.1128/JB.00352-11 21764924.

34. Buensuceso RN, Nguyen Y, Zhang K, Daniel-Ivad M, Sugiman-Marangos SN, Fleetwood AD, et al. The Conserved Tetratricopeptide Repeat-Containing C-Terminal Domain of Pseudomonas aeruginosa FimV Is Required for Its Cyclic AMP-Dependent and -Independent Functions. J Bacteriol. 2016;198(16):2263–74. Epub 2016/06/15. doi: 10.1128/JB.00322-16 27297880.

35. Yamaichi Y, Bruckner R, Ringgaard S, Moll A, Cameron DE, Briegel A, et al. A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev. 2012;26(20):2348–60. Epub 2012/10/17. doi: 10.1101/gad.199869.112 23070816.

36. Fulcher NB, Holliday PM, Klem E, Cann MJ, Wolfgang MC. The Pseudomonas aeruginosa Chp chemosensory system regulates intracellular cAMP levels by modulating adenylate cyclase activity. Mol Microbiol. 2010;76(4):889–904. Epub 2010/03/30. doi: 10.1111/j.1365-2958.2010.07135.x 20345659.

37. Inclan YF, Persat A, Greninger A, Von Dollen J, Johnson J, Krogan N, et al. A scaffold protein connects type IV pili with the Chp chemosensory system to mediate activation of virulence signaling in Pseudomonas aeruginosa. Mol Microbiol. 2016;101(4):590–605. Epub 2016/05/05. doi: 10.1111/mmi.13410 27145134.

38. Saier MH Jr., Feucht BU, McCaman MT. Regulation of intracellular adenosine cyclic 3’:5’-monophosphate levels in Escherichia coli and Salmonella typhimurium. Evidence for energy-dependent excretion of the cyclic nucleotide. J Biol Chem. 1975;250:7593–601. 170265

39. Zhu S, Nishikino T, Hu B, Kojima S, Homma M, Liu J. Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus. Proc Natl Acad Sci U S A. 2017;114(41):10966–71. doi: 10.1073/pnas.1712489114 28973904.

40. Dasgupta N, Arora SK, Ramphal R. fleN, a Gene That Regulates Flagellar Number in Pseudomonas aeruginosa. J Bacteriol. 2000;182(2):357–64. doi: 10.1128/jb.182.2.357-364.2000 10629180

41. Tipping MJ, Delalez NJ, Lim R, Berry RM, Armitage JP. Load-dependent assembly of the bacterial flagellar motor. mBio. 2013;4:e00551–13. doi: 10.1128/mBio.00551-13 23963182

42. Schmidt J, Musken M, Becker T, Magnowska Z, Bertinetti D, Moller S, et al. The Pseudomonas aeruginosa chemotaxis methyltransferase CheR1 impacts on bacterial surface sampling. PLoS One. 2011;6(3):e18184. Epub 2011/03/30. doi: 10.1371/journal.pone.0018184 21445368.

43. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, et al. Second messenger-mediated adjustment of bacterial swimming velocity. Cell. 2010;141:107–16. doi: 10.1016/j.cell.2010.01.018 20303158

44. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol Cell. 2010;38:128–39. doi: 10.1016/j.molcel.2010.03.001 20346719

45. Blair KM, Turner L, Winkelman JT, Berg HC, Kearns DB. A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science. 2008;320(5883):1636–8. Epub 2008/06/21. doi: 10.1126/science.1157877 18566286.

46. Fang X, Gomelsky M. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol. 2010;76(5):1295–305. doi: 10.1111/j.1365-2958.2010.07179.x 20444091.

47. Kojima S, Blair DF. Conformational change in the stator of the bacterial flagellar motor. Biochemistry. 2001;40:13041–50. doi: 10.1021/bi011263o 11669642

48. Zhou J, Lloyd SA, Blair DF. Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc Natl Acad Sci U S A. 1998;95:6436–41. doi: 10.1073/pnas.95.11.6436 9600984

49. Subramanian S, Gao X, Dann CE 3rd, Kearns DB. MotI (DgrA) acts as a molecular clutch on the flagellar stator protein MotA in Bacillus subtilis. Proc Natl Acad Sci U S A. 2017;114(51):13537–42. Epub 2017/12/03. doi: 10.1073/pnas.1716231114 29196522.

50. Leighton TL, Buensuceso RN, Howell PL, Burrows LL. Biogenesis of Pseudomonas aeruginosa type IV pili and regulation of their function. Environ Microbiol. 2015. Epub 2015/03/27. doi: 10.1111/1462-2920.12849 25808785.

51. Luo Y, Zhao K, Baker AE, Kuchma SL, Coggan KA, Wolfgang MC, et al. A hierarchical cascade of second messengers regulates Pseudomonas aeruginosa surface behaviors. mBio. 2015;6(1):e02456–14. Epub 2015/01/30. doi: 10.1128/mBio.02456-14 25626906.

52. Persat A, Inclan YF, Engel JN, Stone HA, Gitai Z. Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2015. Epub 2015/06/05. doi: 10.1073/pnas.1502025112 26041805.

53. Kazmierczak BI, Schniederberend M, Jain R. Cross-regulation of Pseudomonas motility systems: the intimate relationship between flagella, pili and virulence. Curr Opin Microbiol. 2015;28:78–82. doi: 10.1016/j.mib.2015.07.017 26476804.

54. Guttenplan SB, Blair KM, Kearns DB. The EpsE flagellar clutch is bifunctional and synergizes with EPS biosynthesis to promote Bacillus subtilis biofilm formation. PLoS Genet. 2010;6(12):e1001243. Epub 2010/12/21. doi: 10.1371/journal.pgen.1001243 21170308.

55. Wang R, Wang F, He R, Zhang R, Yuan J. The second messenger c-di-GMP adjusts motility and promotes surface aggregation of bacteria. Biophys J. 2018;115:2242–9. doi: 10.1016/j.bpj.2018.10.020 30447993

56. Huangyutitham V, Guvener ZT, Harwood CS. Subcellular clustering of the phosphorylated WspR response regulator protein stimulates its diguanylate cyclase activity. mBio. 2013;4(3):e00242–13. Epub 2013/05/09. doi: 10.1128/mBio.00242-13 23653447.

57. Bennett RR, Lee CK, De Anda J, Nealson KH, Yildiz FH, O'Toole GA, et al. Species-dependent hydrodynamics of flagellum-tethered bacteria in early biofilm development. J R Soc Interface. 2016;13(115):20150966. doi: 10.1098/rsif.2015.0966 26864892.

58. Lee CK, de Anda J, Baker AE, Bennett RR, Luo Y, Lee EY, et al. Multigenerational memory and adaptive adhesion in early bacterial biofilm communities. Proc Natl Acad Sci U S A. 2018;115(17):4471–6. Epub 2018/03/22. doi: 10.1073/pnas.1720071115 29559526.

59. Vogel HJ, Bonner DM. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956;218:97–106. 13278318

60. O'Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R. Genetic approaches to study of biofilms. Methods Enzymol. 1999;310:91–109. doi: 10.1016/s0076-6879(99)10008-9 10547784

61. Jain R, Kazmierczak BI. A Conservative Amino Acid Mutation in the Master Regulator FleQ Renders Pseudomonas aeruginosa Aflagellate. PLoS One. 2014;9(5):e97439. Epub 2014/05/16. doi: 10.1371/journal.pone.0097439 24827992.

62. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 2005;15(10):1451–5. Epub 2005/09/20. doi: 10.1101/gr.4086505 16169926.

63. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754–60. Epub 2009/05/20. doi: 10.1093/bioinformatics/btp324 19451168.

64. Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26(5):589–95. Epub 2010/01/19. doi: 10.1093/bioinformatics/btp698 20080505.

65. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25. Epub 2009/03/06. doi: 10.1186/gb-2009-10-3-r25 19261174.

66. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp352 19505943.

67. Garrity-Ryan L, Kazmierczak B, Kowal R, Comolli J, Hauser A, Engel J. The arginine finger domain of ExoT is required for actin cytoskeleton disruption and inhibition of internalization of Pseudomonas aeruginosa by epithelial cells and macrophages. Infect Immun. 2000;68:7100–13. doi: 10.1128/iai.68.12.7100-7113.2000 11083836

68. de Kerchove AJ, Elimelech M. Impact of alginate conditioning film on deposition kinetics of motile and nonmotile Pseudomonas aeruginosa strains. Appl Environ Microbiol. 2007;73:5227–34. doi: 10.1128/AEM.00678-07 17574995

69. Vallet-Gely I, Donovan KE, Fang R, Joung JK, Dove SL. Repression of phase-variable cup gene expression by H-NS-like proteins in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2005;102(31):11082–7. Epub 2005/07/27. doi: 10.1073/pnas.0502663102 16043713.

70. Dove SL, Hochschild A. Conversion of the omega subunit of Escherichia coli RNA polymerase into a transcriptional activator or an activation target. Genes Dev. 1998;12:745–54. doi: 10.1101/gad.12.5.745 9499408

71. Dufour YS, Gillet S, Frankel NW, Weibel DB, Emonet T. Direct Correlation between Motile Behavior and Protein Abundance in Single Cells. PLoS Comput Biol. 2016;12(9):e1005041. doi: 10.1371/journal.pcbi.1005041 27599206.

72. Parthasarathy R. Rapid, accurate particle tracking by calculation of radial symmetry centers. Nat Methods. 2012;9(7):724–6. Epub 2012/06/13. doi: 10.1038/nmeth.2071 22688415.

73. Jaqaman K, Loerke D, Mettlen M, Kuwata H, Grinstein S, Schmid SL, et al. Robust single-particle tracking in live-cell time-lapse sequences. Nat Methods. 2008;5(8):695–702. Epub 2008/07/22. doi: 10.1038/nmeth.1237 18641657.

74. Theves M, Taktikos J, Zaburdaev V, Stark H, Beta C. A bacterial swimmer with two alternating speeds of propagation. Biophys J. 2013;105(8):1915–24. doi: 10.1016/j.bpj.2013.08.047 24138867.

75. Zhu S, Schniederberend M, Zhitnitsky D, Jain R, Galan JE, Kazmiercak BI, et al. In situ structures of polar and laterla flagella revealed by cryo-electron tomography. J Bacteriol. 2019;201(13):e00117–19. doi: 10.1128/JB.00117-19 31010901

Štítky
Hygiena a epidemiologie Infekční lékařství Laboratoř

Článek vyšel v časopise

PLOS Pathogens


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autoři: MUDr. Tomáš Ürge, PhD.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Aktuální možnosti diagnostiky a léčby AML a MDS nízkého rizika
Autoři: MUDr. Natália Podstavková

Jak diagnostikovat a efektivně léčit CHOPN v roce 2024
Autoři: doc. MUDr. Vladimír Koblížek, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#