Differential proteomic analysis of a polymicrobial biofilm

Journal of Proteome Research

Volumn 11, Issue 9, 2012, Pages 4449-4464

  Zainal Abidin, Zamirah ^a,b   Veith, Paul D ^a   Dashper, Stuart G ^a   Zhu, Ying ^a   Catmull, Deanne V ^a   Chen, Yu Yen ^a   Heryanto, Deasy C ^a   Chen, Dina ^a   Pyke, James S ^a   Tan, Kheng ^a   Mitchell, Helen L ^a   Reynolds, Eric C ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITI KEBANGSAAN MALAYSIA   (Malaysia)

Author keywords

18O; bacterial community; chronic periodontitis; glycine; iron; LC MALDI TOF TOF; Porphyromonas gingivalis; protein secretion; quantitative proteomics; Tannerella forsythia; Treponema denticola

Indexed keywords

BACTERIAL PROTEIN; GLUTAMIC ACID; GLYCINE; PEPTIDASE; PROTEIN HUSA; PROTEIN HUSB; PROTEIN HUSY; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM CULTURE; BIOFILM; LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; POLYMICROBIAL BIOFILM; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

BACTERIAL PROTEINS; BACTEROIDETES; BIOFILMS; CHROMATOGRAPHY, LIQUID; MICROBIAL CONSORTIA; PORPHYROMONAS GINGIVALIS; PROTEOME; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TREPONEMA DENTICOLA;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

EID: 84866114228     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300201c     Document Type: Article

References (93)

1. Hall-Stoodley, L.; Costerton, J. W.; Stoodley, P. Bacterial biofilms: from the natural environment to infectious diseases Nat. Rev. Microbiol. 2004, 2, 95-108 (Pubitemid 39490064)
2. Marsh, P. D. Dental plaque: biological significance of a biofilm and community life-style J. Clin. Periodontol. 2005, 32, 7-15 (Pubitemid 41391052)
3. Roberts, A. P.; Mullany, P. Genetic basis of horizontal gene transfer among oral bacteria Periodontol. 2000 2006, 42, 36-46 (Pubitemid 44286046)
4. Lynch, A. S.; Robertson, G. T. Bacterial and fungal biofilm infections Annu. Rev. Med. 2008, 59, 415-428 (Pubitemid 351287946)
5. 18O reverse proteolytic labeling to determine the effect of biofilm culture on the cell envelope proteome of Porphyromonas gingivalis W50 Proteomics 2008, 8, 1645-1660
6. Lo, A. Comparative transcriptomic analysis of Porphyromonas gingivalis biofilm and planktonic cells BMC Microbiol. 2009, 9, 18
7. Sauer, K. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm J. Bacteriol. 2002, 184, 1140-1154 (Pubitemid 34113383)
8. Kolenbrander, P. E. Oral microbial communities: biofilms,interactions, and genetic systems Annu. Rev. Microbiol. 2000, 54, 413-437
9. Marsh, P. D. Dental plaque as a microbial biofilm Caries Res. 2004, 38, 204-211 (Pubitemid 38716211)
10. Paster, B. J. Bacterial diversity in human subgingival plaque J. Bacteriol. 2001, 183, 3770-3783 (Pubitemid 32510445)
11. Socransky, S. S. Microbial complexes in subgingival plaque J. Clin. Periodontol. 1998, 25, 134-144 (Pubitemid 128705944)
12. Abiko, Y. Profiling of subgingival plaque biofilm microflora from periodontally healthy subjects and from subjects with periodontitis using quantitative real-time PCR J. Periodontal Res. 2010, 45, 389-395
13. Byrne, S. J. Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque Oral Microbiol. Immunol. 2009, 24, 469-477
14. Ximenez-Fyvie, L. A.; Haffajee, A. D.; Socransky, S. S. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis J. Clin. Periodontol. 2000, 27, 648-657
15. Zijnge, V. Oral biofilm architecture on natural teeth PLoS ONE 2010, 5
16. Hajishengallis, G. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement Cell Host Microbe 2011, 10, 497-506
17. Inagaki, S.; Kuramitsu, H. K.; Sharma, A. Contact-dependent regulation of a Tannerella forsythia virulence factor, BspA, in biofilms FEMS Microbiol. Lett. 2005, 249, 291-296 (Pubitemid 41116221)
18. Sharma, A. Synergy between Tannerella forsythia and Fusobacterium nucleatum in biofilm formation Oral Microbiol. Immunol. 2005, 20, 39-42
19. Kuramitsu, H. K.; Chen, W.; Ikegami, A. Biofilm formation by the periodontopathic bacteria Treponema denticola and Porphyromonas gingivalis J. Periodontol. 2005, 76, 2047-2051 (Pubitemid 41748952)
20. Yamada, M.; Ikegami, A.; Kuramitsu, H. K. Synergistic biofilm formation by Treponema denticola and Porphyromonas gingivalis FEMS Microbiol. Lett. 2005, 250, 271-277 (Pubitemid 41188051)
21. Kesavalu, L. Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease Infect. Immun. 2007, 75, 1704-1712 (Pubitemid 46559435)
22. Orth, R. K. Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model Mol. Oral Microbiol. 2011, 26, 229-240
23. Sissons, C. H. Artificial dental plaque biofilm model systems Adv. Dent. Res. 1997, 11, 110-126
24. Davey, M. E.; Duncan, M. J. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis J. Bacteriol. 2006, 188, 5510-5523 (Pubitemid 44157308)
25. Sternberg, C. Distribution of bacterial growth activity in flow-chamber biofilms Appl. Environ. Microbiol. 1999, 65, 4108-4117
26. Resch, A. Comparative proteome analysis of Staphylococcus aureus biofilm and planktonic cells and correlation with transcriptome profiling Proteomics 2006, 6, 1867-1877
27. Shin, J. H. Proteomic analysis of Acinetobacter baumannii in biofilm and planktonic growth mode J. Microbiol. 2009, 47, 728-735
28. Svensäter, G. Protein expression by planktonic and biofilm cells of Streptococcus mutans FEMS Microbiol. Lett. 2001, 205, 139-146 (Pubitemid 33135451)
29. Mitchell, H. L. Treponema denticola biofilm-induced expression of a bacteriophage, toxin-antitoxin systems and transposases Microbiology 2010, 156, 774-788
30. Pham, T. K. A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia Proteomics 2010, 10, 3130-3141
31. Di Cagno, R. Quorum sensing in sourdough Lactobacillus plantarum DC400: induction of plantaricin A (PlnA) under co-cultivation with other lactic acid bacteria and effect of PlnA on bacterial and Caco-2 cells Proteomics 2010, 10, 2175-2190
32. Kuboniwa, M. Proteomics of Porphyromonas gingivalis within a model oral microbial community BMC Microbiol. 2009, 9, 98
33. Orth, R. An efficient method for enumerating oral spirochetes using flow cytometry J. Microbiol. Methods 2010, 80, 123-128
34. Sunde, P. T. Fluorescence in situ hybridization (FISH) for direct visualization of bacteria in periapical lesions of asymptomatic root-filled teeth Microbiology 2003, 149, 1095-1102 (Pubitemid 36636902)
35. Moter, A. Fluorescence in situ hybridization shows spatial distribution of as yet uncultured treponemes in biopsies from digital dermatitis lesions Microbiology 1998, 144, 2459-2467 (Pubitemid 28457154)
36. Heydorn, A. Quantification of biofilm structures by the novel computer program COMSTAT Microbiology 2000, 146, 2395-2407
37. Jacob, H. E.; Norris, J. R.; Ribbons, D. W. Redox potential. In Methods Microbiol, Academic Press: New York, 1970; Vol. 2, pp 91-123.
38. Twigg, R. S. Oxidation-reduction aspects of resazurin Nature 1945, 155, 401-402
39. Sakamoto, M. Rapid detection and quantification of five periodontopathic bacteria by real-time PCR Microbiol. Immunol. 2001, 45, 39-44 (Pubitemid 32142182)
40. Dashper, S. G. Sodium ion-driven serine/threonine transport in Porphyromonas gingivalis J. Bacteriol. 2001, 183, 4142-4148 (Pubitemid 32568064)
41. Molloy, M. P. Extraction of Escherichia coli proteins with organic solvents prior to two-dimensional electrophoresis Electrophoresis 1999, 20, 701-704 (Pubitemid 29222418)
42. O'Brien-Simpson, N. M. An immune response directed to proteinase and adhesin functional epitopes protects against Porphyromonas gingivalis -induced periodontal bone loss J. Immunol. 2005, 175, 3980-3989 (Pubitemid 41292060)
43. Hajkova, D.; Rao, K. C. S.; Miyagi, M. pH dependency of the carboxyl oxygen exchange reaction catalyzed by lysyl endopeptidase and trypsin J. Proteome Res. 2006, 5, 1667-1673 (Pubitemid 44036140)
44. Chen, T. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information Database 2010, 2010, baq013
45. Ishihama, Y. Proteomic LC-MS systems using nanoscale liquid chromatography with tandem mass spectrometry J. Chromatogr. A 2005, 1067, 73-83 (Pubitemid 40363391)
46. Pathirana, R. D. Characterization of proteinase-adhesin complexes of Porphyromonas gingivalis Microbiology 2006, 152, 2381-2394 (Pubitemid 44219645)
47. Seers, C. A. The RgpB C-terminal domain has a role in attachment of RgpB to the outer membrane and belongs to a novel C-terminal-domain family found in Porphyromonas gingivalis J. Bacteriol. 2006, 188, 6376-6386 (Pubitemid 44448580)
48. Chen, Y.-Y. The outer membrane protein LptO is essential for the O-deacylation of LPS and the co-ordinated secretion and attachment of A-LPS and CTD proteins in Porphyromonas gingivalis Mol. Microbiol. 2011, 79, 1380-1401
49. Yu, C. S. Prediction of protein subcellular localization Proteins 2006, 64, 643-651
50. Sanchez, M. C. Structure, viability and bacterial kinetics of an in vitro biofilm model using six bacteria from the subgingival microbiota J. Periodontal Res. 2011, 46, 252-260
51. Standar, K. Setup of an in vitro test system for basic studies on biofilm behavior of mixed-species cultures with dental and periodontal pathogens PLoS ONE 2010, 5
52. Walker, C.; Sedlacek, M. J. An in vitro biofilm model of subgingival plaque Oral Microbiol. Immunol. 2007, 22, 152-161 (Pubitemid 46683963)
53. Davey, M. E. Techniques for the growth of Porphyromonas gingivalis biofilms Periodontol. 2000 2006, 42, 27-35 (Pubitemid 44304235)
54. Oliver, J. D. The viable but nonculturable state in bacteria J. Microbiol. 2005, 43, 93-100 (Pubitemid 40431505)
55. Mineoka, T. Site-specific development of periodontal disease is associated with increased levels of Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia in subgingival plaque J. Periodontol. 2008, 79, 670-676
56. 18O-labeling and tandem mass spectrometry Rapid Commun. Mass Spectrom. 2005, 19, 2259-2271 (Pubitemid 41159732)
57. Jorge, I. Statistical model to analyze quantitative proteomics data obtained by 18O/16O labeling and linear ion trap mass spectrometry: application to the study of vascular endothelial growth factor-induced angiogenesis in endothelial cells Mol. Cell. Proteomics 2009, 8, 1130-1149
58. Bonzon-Kulichenko, E. A robust method for quantitative high-throughput analysis of proteomes by 18O labeling Mol. Cell. Proteomics 2011, 10, M110 003335
59. Dashper, S. G. Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis J. Bacteriol. 2000, 182, 6456-6462
60. Slakeski, N. A Porphyromonas gingivalis genetic locus encoding a heme transport system Oral Microbiol. Immunol. 2000, 15, 388-392
61. Lewis, J. P. Transcriptional organization, regulation and role of the Porphyromonas gingivalis W83 hmu haemin-uptake locus Microbiology 2006, 152, 3367-3382 (Pubitemid 44734339)
62. Olczak, T. Species specificity, surface exposure, protein expression, immunogenicity, and participation in biofilm formation of Porphyromonas gingivalis HmuY BMC Microbiol. 2010, 10, 10
63. Gao, J.-L.; Nguyen, K.-A.; Hunter, N. Characterization of a hemophore-like protein from Porphyromonas gingivalis J. Biol. Chem. 2010, 285, 40028-40038
64. Wójtowicz, H. Unique structure and stability of HmuY, a novel heme-binding protein of Porphyromonas gingivalis PLoS Path. 2009, 5, e1000419
65. Smalley, J. W. HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis PLoS ONE 2011, 6, 10
66. Seshadri, R. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 5646-5651 (Pubitemid 38481210)
67. Xu, X.; Holt, S. C.; Kolodrubetz, D. Cloning and expression of two novel hemin binding protein genes from Treponema denticola Infect. Immun. 2001, 69, 4465-4472 (Pubitemid 32574446)
68. Xu, X. P.; Kolodrubetz, D. Construction and analysis of hemin binding protein mutants in the oral pathogen Treponema denticola Res. Microbiol. 2002, 153, 569-577 (Pubitemid 35223310)
69. Takahashi, N.; Sato, T.; Yamada, T. Metabolic pathways for cytotoxic end product formation from glutamate- and aspartate-containing peptides by Porphyromonas gingivalis J. Bacteriol. 2000, 182, 4704-4710 (Pubitemid 30641789)
70. Grenier, D. Nutritional interactions between two suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis Infect. Immun. 1992, 60, 5298-5301
71. Dashper, S. G. Response of Porphyromonas gingivalis to heme limitation in continuous culture J. Bacteriol. 2009, 191, 1044-1055
72. Veith, P. D. Major proteins and antigens of Treponema denticola Biochim. Biophys. Acta 2009, 1794, 1421-1432
73. Rother, M.; Bock, A.; Wyss, C. Selenium-dependent growth of Treponema denticola: evidence for a clostridial-type glycine reductase Arch. Microbiol. 2001, 177, 113-116 (Pubitemid 34031242)
74. Shah, H. N.; Williams, R. A. D. Utilization of glucose and amino-acids by bacteroides-intermedius and bacteroides-gingivalis Curr. Microbiol. 1987, 15, 241-246
75. Ruby, J. D. Relationship of Treponema denticola periplasmic flagella to irregular cell morphology J. Bacteriol. 1997, 179, 1628-1635 (Pubitemid 27100452)
76. Li, C. Spirochete periplasmic flagella and motility J. Mol. Microbiol. Biotechnol. 2000, 2, 345-354
77. Lux, R. Motility and chemotaxis in tissue penetration of oral epithelial cell layers by Treponema denticola Infect. Immun. 2001, 69, 6276-6283 (Pubitemid 32885192)
78. Li, C. Genetic analysis of spirochete flagellin proteins and their involvement in motility, filament assembly, and flagellar morphology J. Bacteriol. 2008, 190, 5607-5615
79. Wolf, V.; Lange, R.; Wecke, J. Development of quasi-multicellular bodies of Treponema denticola Arch. Microbiol. 1993, 160, 206-213 (Pubitemid 23252499)
80. Veith, P. D. Major outer membrane proteins and proteolytic processing of RgpA and Kgp of Porphyromonas gingivalis W50 Biochem. J. 2002, 363, 105-115 (Pubitemid 34284786)
81. Sato, K. A protein secretion system linked to bacteroidete gliding motility and pathogenesis Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 276-281
82. Curtis, M. A. Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis J. Periodontal Res. 1999, 34, 464-472
83. O'Brien-Simpson, N. M. Role of RgpA, RgpB, and Kgp proteinases in virulence of Porphyromonas gingivalis W50 in a murine lesion model Infect. Immun. 2001, 69, 7527-7534 (Pubitemid 33086579)
84. Frazer, L. T. Vaccination with recombinant adhesins from the RgpA-Kgp proteinase-adhesin complex protects against Porphyromonas gingivalis infection Vaccine 2006, 24, 6542-6554 (Pubitemid 44511855)
85. Haurat, M. F. Selective sorting of cargo proteins into bacterial membrane vesicles J. Biol. Chem. 2011, 286, 1269-1276
86. Mishima, M. Solution structure of the peptidoglycan binding domain of Bacillus subtilis cell wall lytic enzyme CwlC: characterization of the sporulation-related repeats by NMR Biochemistry (Moscow) 2005, 44, 10153-10163 (Pubitemid 41076810)
87. Coats, S. R. The lipid A phosphate position determines differential host Toll-like receptor 4 responses to phylogenetically related symbiotic and pathogenic bacteria Infect. Immun. 2011, 79, 203-210
88. Gerber, A.; Krell, S.; Morenz, J. Recombinant Treponema pallidum antigens in syphilis serology Immunobiology 1996, 196, 535-549 (Pubitemid 27168446)
89. Schouls, L. M.; van der Heide, H. G.; van Embden, J. D. Characterization of the 35-kilodalton Treponema pallidum subsp. pallidum recombinant lipoprotein TmpC and antibody response to lipidated and nonlipidated T. pallidum antigens Infect. Immun. 1991, 59, 3536-3546
90. Chu, L. Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities Infect. Immun. 1997, 65, 3231-3238 (Pubitemid 27342404)
91. Johnson, N. A.; Liu, Y.; Fletcher, H. M. Alkyl hydroperoxide peroxidase subunit C (ahpC) protects against organic peroxides but does not affect the virulence of Porphyromonas gingivalis W83 Oral Microbiol. Immunol. 2004, 19, 233-239 (Pubitemid 38931706)
92. Kvint, K. The bacterial universal stress protein: function and regulation Curr. Opin. Microbiol. 2003, 6, 140-145 (Pubitemid 36628657)
93. Chen, W. A universal stress protein of Porphyromonas gingivalis is involved in stress responses and biofilm formation FEMS Microbiol. Lett 2006, 264, 15-21 (Pubitemid 44511049)