The new flagella-associated collagen-like proteins ClpB and ClpC of Bacillus amyloliquefaciens FZB42 are involved in bacterial motility

Microbiological Research

Volumn 184, Issue , 2016, Pages 25-31

  Zhao, Xia ^a,b,c   Wang, Ruoyu ^a,c   Shang, Qianhan ^a,b,c   Hao, Haiting ^a,b,c   Li, Yuyao ^d   Zhang, Yubao ^a,c   Guo, Zhihong ^a,c   Wang, Yun ^a   Xie, Zhongkui ^a,c  

^a Chinese Academy of Sciences   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c Gansu Provincial Key Laboratory of Digestive System Tumors   (China)

^d LANZHOU UNIVERSITY   (China)

Author keywords

Bacteria motility; Collagen like proteins; Flagella; Immunogold labeling; Plant growth promoting rhizobacteria

Indexed keywords

BACTERIOLOGY; BIOFILMS; CELL MEMBRANES; CELLS; COLLAGEN; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; PLANTS (BOTANY); PROTEINS; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; BACILLUS AMYLOLIQUEFACIENS; EXTRACELLULAR MATRICES; FLAGELLA; N-AND C-TERMINAL DOMAINS; PLANT GROWTH PROMOTING; PLANT GROWTH PROMOTING RHIZOBACTERIA; WILD-TYPE BACTERIA;

BACTERIA;

AGAR; AMINO ACID; BACTERIUM; BIOFILM; COLLAGEN; GENE EXPRESSION; MOTILITY; RHIZOBACTERIUM;

ANIMALIA; BACILLUS AMYLOLIQUEFACIENS; BACTERIA (MICROORGANISMS); RHIZOBIALES; RHIZOBIUM;

BACTERIAL PROTEIN; MEMBRANE PROTEIN;

BACILLUS; CHEMISTRY; FLAGELLUM; GENE INACTIVATION; GENETICS; IMMUNOELECTRON MICROSCOPY; LOCOMOTION; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

BACILLUS; BACTERIAL PROTEINS; FLAGELLA; GENE KNOCKOUT TECHNIQUES; LOCOMOTION; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, IMMUNOELECTRON;

EID: 84957575881     PISSN: 09445013     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micres.2015.12.004     Document Type: Article

References (57)

1. Alan J., Robin T. Immunochemistry in Practice 1982, Blackwell Scientific Publications Ltd., Barry street, Carlton,Victoria 3053, Australia.
2. Boydston J.A., Chen P., Steichen C.T., Turnbough C.L. Orientation within the exosporium and structural stability of the collagen-like glycoprotein BclA of Bacillus anthracis. J. Bacteriol. 2005, 187:5310-5317.
3. Chen X.H., Vater J., Piel J., et al. Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. J. Bacteriol. 2006, 188:4024-4036.
4. Chen X.H., Koumoutsi A., Scholz R., et al. Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nat. Biotechnol. 2007, 25:1007-1014.
5. Chiang P., Habash M., Burrows L.L. Disparate subcellular localization patterns of Pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J. Bacteriol. 2005, 187:829-839.
6. Chin-A-Woeng T.F.C., Bloemberg G.V., Mulders I.H.M., Dekkers L.C., Lugtenberg B.J.J. Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol. Plant Microbe Interact. 2000, 13:1340-1345.
7. Correa N.E., Peng F., Klose K.E. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J. Bacteriol. 2005, 187:6324-6332.
8. Darzins A. Characterization of a Pseudomonas-aeruginosa gene-cluster involved in pilus biosynthesis and twitching motility-sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus-xanthus. Mol. Microbiol. 1994, 11:137-153.
9. Dasgupta N., Arora S.K., Ramphal R. fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 2000, 182:357-364.
10. Duncan C., Prashar A., So J., Tang P., Low D.E., Terebiznik M., Guyard C. Lcl of Legionella pneumophila is an immunogenic GAG binding adhesin that promotes interactions with lung epithelial cells and plays a crucial role in biofilm formation. Infect. Immun. 2011, 79:2168-2181.
11. Engel J., Bachinger H.P. Collagen-like sequences in phages and bacteria. Proceedings of the Indian Academy of Sciences-Chemical Sciences. Springer India 1999, 111:81-86.
12. Erickson P.R., Herzberg M.C. A collagen-like immunodeterminant on the surface of Streptococcus-sanguis induces platelet-aggregation. J. Immunol. 1987, 138:3360-3366.
13. Fan B., Chen X.H., Budiharjo A., Bleiss W., Vater J., Borriss R. Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. J. Biotechnol. 2011, 151:303-311.
14. Fan B., Borriss R., Bleiss W., Wu X.Q. Gram-positive rhizobacterium Bacillus amyloliquefaciens FZB42 colonizes three types of plants in different patterns. J. Microbiol. 2012, 50:38-44.
15. Guttenplan S.B., Shaw S., Kearns D.B. The cell biology of peritrichous flagella in Bacillus subtilis. Mol. Microbiol. 2013, 87:211-229.
16. Idris E.E., Iglesias D.J., Talon M., Borriss R. Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol. Plant Microbe Interact. 2007, 20:619-626.
17. Idriss E.E., Makarewicz O., Farouk A., Rosner K., Greiner R., Bochow H., Richter T., Borriss R. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 2002, 148:2097-2109.
18. Julkowska D., Obuchowski M., Holland I.B., Seror S.J. Comparative analysis of the development of swarming communities of Bacillus subtilis 168 and a natural wild type: critical effects of surfactin and the composition of the medium. J. Bacteriol. 2005, 187:65-76.
19. Jung H.-C., Park J.-H., Park S.-H., Lebeault J.-M., Pan J.-G. Expression of carboxymethylcellulase on the surface of E. coli using Pseudomonas syringae ice nucleation protein. Enzyme Microb. Technol. 1998, 22:348-354.
20. Kadler K.E., Baldock C., Bella J., Boot-Handford R.P. Collagens at a glance. J. Cell Sci. 2007, 120:1955-1958.
21. Kohler T., Curty L.K., Barja F., van Delden C., Pechere J.C. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 2000, 182:5990-5996.
22. Koumoutsi A., Chen X.H., Henne A., Liesegang H., Hitzeroth G., Franke P., Vater J., Borriss R. Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J. Bacteriol. 2004, 186:1084-1096.
23. Lukomski S., Nakashima K., Abdi I., Cipriano V.J., Ireland R.M., Reid S.D., Adams G.G., Musser J.M. Identification and characterization of the scl gene encoding a group A Streptococcus extracellular protein virulence factor with similarity to human collagen. Infect. Immun. 2000, 68:6542-6553.
24. MacKichan J.K., Gerns H.L., Chen Y.-T., Zhang P., Koehler J.E. A SacB mutagenesis strategy reveals that the Bartonella quintana variably expressed outer membrane proteins are required for bloodstream infection of the host. Infect. Immun. 2008, 76:788-795.
25. Mallegol J., Duncan C., Prashar A., So J., Low D.E., Terebeznik M., Guyard C. Essential roles and regulation of the Legionella pneumophila collagen-like adhesin during biofilm formation. PLoS One 2012, 7:e46462.
26. Moens S., Vanderleyden J. Functions of bacterial flagella. Crit. Rev. Microbiol. 1996, 22:67-100.
27. Navarre W.W., Schneewind O. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 1999, 63:174-229.
28. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
29. O'Toole G.A., Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 1998, 30:295-304.
30. Oliver-Kozup H., Martin K.H., Schwegler-Berry D., Green B.J., Betts C., Shinde A.V., Van De Water L., Lukomski S. The group A streptococcal collagen-like protein-1, Scl1, mediates biofilm formation by targeting the extra domain A-containing variant of cellular fibronectin expressed in wounded tissue. Mol. Microbiol. 2013, 87:672-689.
31. Oliver-Kozup H.A., Elliott M., Bachert B.A., Martin K.H., Reid S.D., Schwegler-Berry D.E., Green B.J., Lukomski S. The streptococcal collagen-like protein-1 (Scl1) is a significant determinant for biofilm formation by group a Streptococcus. BMC Microbiol. 2011, 11:262.
32. Park T.J., Heo N.S., Yim S.S., Park J.H., Jeong K.J., Lee S.Y. Surface display of recombinant proteins on E. coli by BclA exosporium of Bacillus anthracis. Microb. Cell Fact. 2013, 12.
33. Patrick J.E., Kearns D.B. Swarming motility and the control of master regulators of flagellar biosynthesis. Mol. Microbiol. 2012, 83:14-23.
34. Pratt L.A., Kolter R. Genetic analysis of E. coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 1998, 30:285-293.
35. Pugsley A.P. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 1993, 57:50.
36. Rashid M.H., Kornberg A. Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc. Nat. Acad. Sci. U. S. A. 2000, 97:4885-4890.
37. Roberts F., Doetsch R. Some singular properties of bacterial flagella: with special reference to monotrichous forms. J. Bacteriol. 1966, 91:414-421.
38. Romero D., Aguilar C., Losick R., Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Nat. Acad. Sci. 2010, 107:2230-2234.
39. Serra D.O., Richter A.M., Klauck G., Mika F., Hengge R. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. mBio 2013, 4:e00103-e00113.
40. Silverman M., Simon M.I. Bacterial flagella. Ann. Rev. Microbiol. 1977, 31:397-419.
41. Smith M.C.M., Burns R.N., Wilson S.E., Gregory M.A. The complete genome sequence of the Streptomyces temperate phage phi C31 evolutionary relationships to other viruses. Nucleic Acids Res. 1999, 27:2145-2155.
42. Sun L.L., Jin M., Ding W., Yuan J., Kelly J., Gao H.C. Posttranslational modification of flagellin FlaB in Shewanella oneidensis. J. Bacteriol. 2013, 195:2550-2561.
43. Sylvestre P., Couture-Tosi E., Mock M. A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol. Microbiol. 2002, 45:169-178.
44. Sylvestre P., Couture-Tosi E., Mock M. Polymorphism in the collagen-like region of the Bacillus anthracis BclA protein leads to variation in exosporium filament length. J. Bacteriol. 2003, 185:1555-1563.
45. Sylvestre P., Couture-Tosi E., Mock M. Contribution of ExsFA and ExsFB proteins to the localization of BclA on the spore surface and to the stability of the Bacillus anthracis exosporium. J. Bacteriol. 2005, 187:5122-5128.
46. Thompson B.M., Waller L.N., Fox K.F., Fox A., Stewart G.C. The BclB glycoprotein of Bacillus anthracis is involved in exosporium integrity. J. Bacteriol. 2007, 189:6704-6713.
47. Thompson B.M., Stewart G.C. Targeting of the BclA and BclB proteins to the Bacillus anthracis spore surface. Mol. Microbiol. 2008, 70:421-434.
48. Tomich M., Mohr C.D. Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS Microbiol. Lett. 2003, 228:287-297.
49. Watnick P.I., Lauriano C.M., Klose K.E., Croal L., Kolter R. The absence of a flagellum leads to altered colony morphology: biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 2001, 39:223-235.
50. Whatmore A.M. Streptococcus pyogenes sclB encodes a putative hypervariable surface protein with a collagen-like repetitive structure. Microbiology 2001, 147:419-429.
51. Whitchurch C.B., Hobbs M., Livingston S.P., Krishnapillai V., Mattick J.S. Characterization of a Pseudomonas-aeruginosa twitching motility gene and evidence for a specialized protein export system widespread in eubacteria. Gene 1991, 101:33-44.
52. Wolber P.K., Deininger C.A., Southworth M.W., Vandekerckhove J., Van Montagu M., Warren G.J. Identification and purification of a bacterial ice-nucleation protein. Proc. Nat. Acad. Sci. 1986, 83:7256-7260.
53. Wood T.K., Barrios A.F.G., Herzberg M., Lee J. Motility influences biofilm architecture in E. coli. Appl. Microbiol. Biotnol. 2006, 72:361-367.
54. Xu Y., Keene D.R., Bujnicki J.M., Hook M., Lukomski S. Streptococcal Scl1 and Scl2 proteins form collagen-like triple helices. J. Biol. Chem. 2002, 277:27312-27318.
55. Yoshizumi A., Yu Z.X., Silva T., Thiagarajan G., Ramshaw J.A.M., Inouye M., Brodsky B. Self-association of Streptococcus pyogenes collagen-like constructs into higher order structures. Protein Sci. 2009, 18:1241-1251.
56. Zhao X., Wang Y., Shang Q., et al. Collagen-Like Proteins (ClpA, ClpB, ClpC, and ClpD) are required for biofilm formation and adhesion to plant roots by Bacillus amyloliquefaciens FZB42. PLoS One 2015, 10:e0117414.
57. Zogaj X., Nimtz M., Rohde M., Bokranz W., Römling U. The multicellular morphotypes of Salmonella typhimurium and E. coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 2001, 39:1452-1463.