Collagen-like proteins (ClpA, ClpB, ClpC, and ClpD) are required for biofilm formation and adhesion to plant roots by Bacillus amyloliquefaciens FZB42

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

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

^a Chinese Academy of Sciences   (China)

^b Key Laboratory of Stress Physiology and Ecology in Cold and Arid Regions of Gansu Province   (China)

^c LANZHOU UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN LIKE PROTEIN A; COLLAGEN LIKE PROTEIN B; COLLAGEN LIKE PROTEIN C; COLLAGEN LIKE PROTEIN D; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CLPC PROTEIN, BACTERIA; HEAT SHOCK PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; BACILLUS AMYLOLIQUEFACIENS; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BIOFILM; CELL SHAPE; CELL STRUCTURE; CELL SURFACE; CELL WALL; CONTROLLED STUDY; FLAGELLUM; HYDROPHOBICITY; NONHUMAN; OUTER MEMBRANE; PHENOTYPE; PLANT MICROORGANISM INTERACTION; PLANT ROOT; PROTEIN FUNCTION; PROTEIN STRUCTURE; SCANNING ELECTRON MICROSCOPY; AMINO ACID SEQUENCE; ARABIDOPSIS; BACILLUS; BACTERIAL GENOME; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYSIOLOGY; PLASMID; PROTEIN TERTIARY STRUCTURE;

ARABIDOPSIS THALIANA; BACILLUS (BACTERIUM); BACILLUS AMYLOLIQUEFACIENS; BACILLUS CEREUS; BACTERIA (MICROORGANISMS); RHIZOBIALES;

AMINO ACID SEQUENCE; ARABIDOPSIS; BACILLUS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; GENOME, BACTERIAL; HEAT-SHOCK PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; PLANT ROOTS; PLASMIDS; PROTEIN STRUCTURE, TERTIARY;

EID: 84922575736     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117414     Document Type: Article

References (58)

1. Vercellotti G, McCarthy J, Lindholm P, Peterson P, Jacob H, et al. (1985) Extracellular matrix proteins (fibronectin, laminin, and type IV collagen) bind and aggregate bacteria. The American journal of pathology 120: 13. PMID: 4014440
2. Kadler KE, Baldock C, Bella J, Boot-Handford RP (2007) Collagens at a glance. Journal of Cell Science 120: 1955-1958. PMID: 17550969
3. Knott L, Bailey A (1998) Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 22: 181-187. PMID: 9514209
4. Liotta L, Tryggvason K, Garbisa S, Hart I, Foltz C, et al. (1980) Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284: 67-68. PMID: 6243750
5. Tayapad JB, Viguilla AQ, Reyes JM (2013) Collagen cross-linking and corneal infections. Current opinion in ophthalmology 24: 288-290. doi: 10.1097/ICU.0b013e32836229c5 PMID: 23703462
6. Yu Z, An B, Ramshaw JA, Brodsky B (2014) Bacterial collagen-like proteins that form triple-helical structures. Journal of structural biology. doi: 10.1016/j.jsb.2015.01.001 PMID: 25592778
7. Rasmussen M, Jacobsson M, Bjorck L (2003) Genome-based identification and analysis of collagenrelated structural motifs in bacterial and viral proteins. Journal of Biological Chemistry 278: 32313-32316. PMID: 12788919
8. Sylvestre P, Couture-Tosi E, Mock M (2002) A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Molecular Microbiology 45: 169-178. PMID: 12100557
9. Steichen CT, Kearney JF, Turnbough CL (2005) Characterization of the exosporium basal layer protein BxpB of Bacillus anthracis. Journal of Bacteriology 187: 5868-5876. PMID: 16109927
10. Thompson BM, Stewart GC (2008) Targeting of the BclA and BclB proteins to the Bacillus anthracis spore surface. Molecular Microbiology 70: 421-434. doi: 10.1111/j.1365-2958.2008.06420.x PMID: 18761690
11. Erickson PR, Herzberg MC (1987) A Collagen-Like Immunodeterminant on the Surface of Streptococcus-Sanguis Induces Platelet-Aggregation. Journal of Immunology 138: 3360-3366. PMID: 2437190
12. Lukomski S, Nakashima K, Abdi I, Cipriano VJ, Shelvin BJ, et al. (2001) Identification and characterization of a second extracellular collagen-like protein made by group A Streptococcus: Control of production at the level of translation. Infection and Immunity 69: 1729-1738. PMID: 11179350
13. Abdel-Nour M, Duncan C, Prashar A, Rao C, Ginevra C, et al. (2014) The Legionella pneumophila Collagen-Like Protein Mediates Sedimentation, Autoaggregation, and Pathogen-Phagocyte Interactions. Applied and environmental microbiology 80: 1441-1454. doi: 10.1128/AEM.03254-13 PMID: 24334670
14. Dinkla K, Rohde M, Jansen WMT, Carapetis JR, Chhatwal GS, et al. (2003) Streptococcus pyogenes recruits collagen via surface-bound fibronectin: a novel colonization and immune evasion mechanism. Molecular Microbiology 47: 861-869. PMID: 12535082
15. Cho KH, Caparon MG (2005) Patterns of virulence gene expression differ between biofilm and tissue communities of Streptococcus pyogenes. Molecular Microbiology 57: 1545-1556. PMID: 16135223
16. Oliver-Kozup HA, Elliott M, Bachert BA, Martin KH, Reid SD, et al. (2011) The streptococcal collagenlike protein-1 (Scl1) is a significant determinant for biofilm formation by group a Streptococcus. Bmc Microbiology 11. doi: 10.1186/1471-2180-11-269 PMID: 22208551
17. Mallegol J, Duncan C, Prashar A, So J, Low DE, et al. (2012) Essential Roles and Regulation of the Legionella pneumophila Collagen-Like Adhesin during Biofilm Formation. Plos One 7: e46462. doi: 10.1371/journal.pone.0046462 PMID: 23029523
18. Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, et al. (2007) Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nature Biotechnology 25: 1007-1014. PMID: 17704766
19. Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Molecular Plant-Microbe Interactions 20: 619-626. PMID: 17555270
20. Chen XH, Vater J, Piel J, Franke P, Scholz R, et al. (2006) Structural and functional characterization of three polyketide synthase gene clusters in Bacillus amyloliquefaciens FZB 42. Journal of Bacteriology 188: 4024-4036. PMID: 16707694
21. Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, et al. (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. Journal of Bacteriology 186: 1084-1096. PMID: 14762003
22. Makarewicz I, Dubrac S, Msadek T, Borriss R (2006) Dual role of the PhoP similar to P response regulator: Bacillus amyloliquefaciens FZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. Journal of Bacteriology 188: 6953-6965. PMID: 16980498
23. Rasmussen M, Edén A, Björck L (2000) SclA, a Novel Collagen-Like Surface Protein of Streptococcus pyogenes. Infection and immunity 68: 6370-6377. PMID: 11035747
24. Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. Journal of bacteriology 186: 4427-4440. PMID: 15231774
25. Espinosa-Urgel M, Kolter R, Ramos J-L (2002) Root colonization by Pseudomonas putida: love at first sight. Microbiology 148: 341-343. PMID: 11832496
26. Walker TS, Bais HP, Déziel E, Schweizer HP, Rahme LG, et al. (2004) Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant physiology 134: 320-331. PMID: 14701912
27. Ramey BE, Koutsoudis M, von Bodman SB, Fuqua C (2004) Biofilm formation in plant-microbe associations. Current opinion in microbiology 7: 602-609. PMID: 15556032
28. Fan B, Chen XH, Budiharjo A, Bleiss W, Vater J, et al. (2011) Efficient colonization of plant roots by the plant growth promoting bacterium Bacillus amyloliquefaciens FZB42, engineered to express green fluorescent protein. Journal of Biotechnology 151: 303-311. doi: 10.1016/j.jbiotec.2010.12.022 PMID: 21237217
29. Fan B, Borriss R, Bleiss W, Wu XQ (2012) Gram-positive Rhizobacterium Bacillus amyloliquefaciens FZB42 Colonizes Three Types of Plants in Different Patterns. Journal of Microbiology 50: 38-44. doi: 10.1007/s12275-012-1439-4 PMID: 22367935
30. Fan B, Carvalhais LC, Becker A, Fedoseyenko D, von Wiren N, et al. (2012) Transcriptomic profiling of Bacillus amyloliquefaciens FZB42 in response to maize root exudates. Bmc Microbiology 12. doi: 10.1186/1471-2180-12-307 PMID: 23272650
31. Dietel K, Beator B, Budiharjo A, Fan B, Borriss R (2013) Bacterial traits involved in colonization of Arabidopsis thaliana roots by Bacillus amyloliquefaciens FZB42. Plant Pathol J 29: 59-66. doi: 10.5423/PPJ.OA.10.2012.0155 PMID: 25288929
32. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Molecular microbiology 59: 1229-1238. PMID: 16430696
33. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proceedings of the National Academy of Sciences 107: 2230-2234. doi: 10.1073/pnas.0910560107 PMID: 20080671
34. Sheng G-P, Yu H-Q, Li X-Y (2010) Extracellular polymeric substances (EPS) of microbial aggregates in biological wastewater treatment systems: a review. Biotechnology Advances 28: 882-894. doi: 10.1016/j.biotechadv.2010.08.001 PMID: 20705128
35. Kunst F, Rapoport G (1995) Salt Stress Is an Environmental Signal Affecting Degradative Enzyme-Synthesis in Bacillus-Subtilis. Journal of Bacteriology 177: 2403-2407. PMID: 7730271
36. O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Molecular microbiology 28: 449-461. PMID: 9632250
37. O'Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, et al. (1999) Genetic approaches to study of biofilms.
38. Piao Z, Sze CC, Barysheva O, Iida K-I, Yoshida S-I (2006) Temperature-regulated formation of mycelial mat-like biofilms by Legionella pneumophila. Applied and environmental microbiology 72: 1613-1622. PMID: 16461717
39. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Molecular microbiology 42: 1199-1209. PMID: 11886552
40. Pan W-H, Li P-L, Liu Z (2006) The correlation between surface hydrophobicity and adherence of Bifidobacterium strains from centenarians' faeces. Anaerobe 12: 148-152. PMID: 16765861
41. Recorbet G, Alabouvette C (1997) Adhesion of Fusarium oxysporum conidia to tomato roots. Letters in Applied Microbiology 25: 375-379.
42. Becherelli M, Manetti AG, Buccato S, Viciani E, Ciucchi L, et al. (2012) The ancillary protein 1 of Streptococcus pyogenes FCT-1 pili mediates cell adhesion and biofilm formation through heterophilic as well as homophilic interactions. Molecular microbiology 83: 1035-1047. doi: 10.1111/j.1365-2958.2012. 07987.x PMID: 22320452
43. Chagnot C, Agus A, Renier S, Peyrin F, Talon R, et al. (2013) In Vitro Colonization of the Muscle Extracellular Matrix Components by Escherichia coli O157:H7: The Influence of Growth Medium, Temperature and pH on Initial Adhesion and Induction of Biofilm Formation by Collagens I and III. Plos One 8: e59386. doi: 10.1371/journal.pone.0059386 PMID: 23516631
44. Dickson JS, Koohmaraie M (1989) Cell-Surface Charge Characteristics and Their Relationship to Bacterial Attachment to Meat Surfaces. Applied and Environmental Microbiology 55: 832-836. PMID: 2499255
45. Gusils C, Cuozzo S, Sesma F, Gonzalez S (2002) Examination of adhesive determinants in three species of Lactobacillus isolated from chicken. Canadian Journal of Microbiology 48: 34-42. PMID: 11888161
46. Ahimou F, Paquot M, Jacques P, Thonart P, Rouxhet PG (2001) Influence of electrical properties on the evaluation of the surface hydrophobicity of Bacillus subtilis. Journal of Microbiological Methods 45: 119-126. PMID: 11311397
47. Xu Y, Keene DR, Bujnicki JM, Hook M, Lukomski S (2002) Streptococcal Scl1 and Scl2 proteins form collagen-like triple helices. Journal of Biological Chemistry 277: 27312-27318. PMID: 11976327
48. Ghosh N, McKillop TJ, Jowitt TA, Howard M, Davies H, et al. (2012) Collagen-like proteins in pathogenic E. coli strains. PloS one 7: e37872. doi: 10.1371/journal.pone.0037872 PMID: 22701585
49. Yoshizumi A, Yu ZX, Silva T, Thiagarajan G, Ramshaw JAM, et al. (2009) Self-association of Streptococcus pyogenes collagen-like constructs into higher order structures. Protein Science 18: 1241-1251. doi: 10.1002/pro.134 PMID: 19472339
50. Boydston JA, Yue L, Kearney JF, Turnbough CL (2006) The ExsY protein is required for complete formation of the exosporium of Bacillus anthracis. Journal of Bacteriology 188: 7440-7448. PMID: 16936017
51. Thompson BM, Waller LN, Fox KF, Fox A, Stewart GC (2007) The BclB glycoprotein of Bacillus anthracis is involved in exosporium integrity. Journal of Bacteriology 189: 6704-6713. PMID: 17644587
52. Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton J, et al. (1998) The involvement of cell-tocell signals in the development of a bacterial biofilm. Science 280: 295-298. PMID: 9535661
53. Xue QO, Gu CF, Rivera J, Hook M, Chen XW, et al. (2011) Entry of Bacillus anthracis spores into epithelial cells is mediated by the spore surface protein BclA, integrin alpha 2 beta 1 and complement component C1q. Cellular Microbiology 13: 620-634. doi: 10.1111/j.1462-5822.2010.01558.x PMID: 21134100
54. Courtney HS, Ofek I, Penfound T, Nizet V, Pence MA, et al. (2009) Relationship between expression of the family of M proteins and lipoteichoic acid to hydrophobicity and biofilm formation in Streptococcus pyogenes. PLoS One 4: e4166. doi: 10.1371/journal.pone.0004166 PMID: 19132104
55. Abdel-Nour M, Duncan C, Prashar A, Rao C, Ginevra C, et al. (2013) The Legionella pneumophila collagen-like protein mediates sedimentation, auto-aggregation and pathogen-phagocyte interactions. Applied and Environmental Microbiology: AEM. 03254-03213.
56. Felek S, Lawrenz MB, Krukonis ES (2008) The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology 154: 1802-1812. doi: 10.1099/mic.0. 2007/010918-0 PMID: 18524935
57. Tomich M, Mohr CD (2003) Adherence and autoaggregation phenotypes of a Burkholderia cenocepacia cable pilus mutant. FEMS microbiology letters 228: 287-297. PMID: 14638436
58. MacKichan JK, Gerns HL, Chen Y-T, Zhang P, Koehler JE (2008) A SacB mutagenesis strategy reveals that the Bartonella quintana variably expressed outer membrane proteins are required for bloodstream infection of the host. Infection and immunity 76: 788-795. PMID: 18070893