| BMC Microbiology | |
| Proteomics of Streptococcus gordonii within a model developing oral microbial community | |
| Murray Hackett4  Richard J Lamont1  Christopher J Wright1  Sarah E Whitmore1  Brittany C Dickinson2  Tiansong Wang3  Erik L Hendrickson4  | |
| [1] Center for Oral Health and Systemic Disease, University of Louisville, Louisville, KY, 40292, USA;Department of Oral Biology, University of Florida, Gainesville, FL, 32610, USA;Department of Microbiology, University of Washington, Box 357242, Seattle, WA, 98195, USA;Department of Chemical Engineering, University of Washington, Box 355014, Seattle, WA, 98195, USA | |
| 关键词: Fusobacterium nucleatum; Porphyromonas gingivalis; Model community; Proteomics; Oral biofilm; Streptococcus gordonii; | |
| Others : 1221752 DOI : 10.1186/1471-2180-12-211 |
|
| received in 2012-05-15, accepted in 2012-09-17, 发布年份 2012 | |
PDF
|
|
【 摘 要 】
Background
Streptococcus gordonii is one of several species that can initiate the formation of oral biofilms that develop into the complex multispecies microbial communities referred to as dental plaque. It is in the context of dental plaque that periodontal pathogens such as Porphyromonas gingivalis cause disease. We have previously reported a whole cell quantitative proteomics investigation of P. gingivalis in a model dental plaque community of S. gordonii, P. gingivalis, and Fusobacterium nucleatum. Here we report the adaptation of S. gordonii to the same model.
Results
1122 S. gordonii proteins were detected in S. gordonii control samples, 915 in communities with F. nucleatum, 849 with P. gingivalis, and 649 with all three organisms. Quantitative comparisons showed extensive proteome changes in association with F. nucleatum or P. gingivalis individually or both P. gingivalis and F. nucleatum together. The changes were species specific, though the P. gingivalis interaction may be dominant, indicated by large differences between the proteomes with F. nucleatum or P. gingivalis but limited changes between communities with P. gingivalis or both P. gingivalis and F. nucleatum. The results were inspected manually and an ontology analysis conducted using DAVID. Extensive changes were seen in nutrition pathways with increases in energy metabolism and changes in the resulting byproducts, while the acid and sugar repressed PTS (phosphoenolpyruvate dependent phosphotransferase system) sugar transport systems showed decreases. These results were seen across all the multispecies samples, though with different profiles according to the partner species. F. nucleatum association decreased proteins for the metabolic end products acetate and ethanol but increased lactate, the primary source of acidity from streptococcal cultures. P. gingivalis containing samples had a reduction in levels of proteins for ethanol and formate but increased proteins for both acetate and lactate production. The communities also showed increases in exopolysaccharide synthesis, amino acid biosynthesis, and oxidative stress protection and decreases in adhesion and transporter proteins.
Conclusion
This study showed that S. gordonii demonstrates species specific responses during interactions with F. nucleatum or P. gingivalis. Extensive changes were seen in energy metabolism and byproduct production implicating nutrient transfer as an important community interaction.
【 授权许可】
2012 Hendrickson et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
|---|---|---|---|
| 20150803112703383.pdf | 2811KB | ||
| Figure 13. | 102KB | Image | |
| Figure 12. | 96KB | Image | |
| Figure 11. | 104KB | Image | |
| Figure 10. | 101KB | Image | |
| Figure 9. | 104KB | Image | |
| Figure 8. | 103KB | Image | |
| Figure 7. | 90KB | Image | |
| Figure 6. | 89KB | Image | |
| Figure 5. | 91KB | Image | |
| Figure 4. | 92KB | Image | |
| Figure 3. | 100KB | Image | |
| Figure 2. | 91KB | Image | |
| Figure 1. | 126KB | Image |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.
Figure 10.
Figure 11.
Figure 12.
Figure 13.
【 参考文献 】
- [1]Nyvad B, Kilian M: Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand J Dent Res 1987, 95:369-380.
- [2]Kolenbrander PE, London J: Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 1993, 175:3247-3252.
- [3]Bradshaw DJ, Marsh PD: Analysis of pH-Driven Disruption of Oral Microbial Communities in vitro. Caries Res 1998, 32:456-462.
- [4]Kolenbrander PE, Andersen RN, Moore LV: Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix. Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun 1989, 57:3194-3203.
- [5]Park Y, Simionato MR, Sekiya K, Murakami Y, James D, Chen W, Hackett M, Yoshimura F, Demuth DR, Lamont RJ: Short Fimbriae of Porphyromonas gingivalis and Their Role in Coadhesion with Streptococcus gordonii. Infect Immun 2005, 73:3983-3989.
- [6]Periasamy S, Kolenbrander PE: Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 2009, 191:6804-6811.
- [7]Ramsey MM, Rumbaugh KP, Whiteley M: Metabolite Cross-Feeding Enhances Virulence in a Model Polymicrobial Infection. PLoS Pathogens 2011, 7:e1002012.
- [8]Loesche WJ: Role of Streptococcus mutans in Human Dental Decay. Microbiol Rev 1986, 50:353-380.
- [9]de Soet JJ, Nyvad B, Kilian M: Strain-Related Acid Production by Oral Streptococci. Caries Res 2000 1999, 34:486-490.
- [10]Merritt J, Kreth J, Shi W, Qi F: LuxS controls bacteriocin production in Streptococcus mutans through a novel regulatory component. Mol Microbiol 2005, 57:960-969.
- [11]Kuboniwa M, Hendrickson EL, Xia Q, Wang T, Xie H, Hackett M, Lamont RJ: Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol 2009, 9:98. BioMed Central Full Text
- [12]Kuboniwa M, Lamont RJ: Subgingival biofilm formation. Periodontol 2010, 52:38-52.
- [13]Kuramitsu HK, He X, Lux R, Anderson MH, Shi W: Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 2007, 71:653-670.
- [14]Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS: Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 2010, 8:471-480.
- [15]Jenkinson HF, Lamont RJ: Oral microbial communities in sickness and in health. Trends Microbiol 2005, 13:589-595.
- [16]Whitmore SE, Lamont RJ: The pathogenic persona of community-associated oral streptococci. Mol Microbiol 2011, 81:305-314.
- [17]Jacobson GR, Lodge J, Poy F: Carbohydrate uptake in the oral pathogen Streptococcus mutans: mechanisms and regulation by protein phosphorylation. Biochimie 1989, 71:997-1004.
- [18]Mikx FHM, van der Hoeven JS: Symbiosis of Streptococcus mutans and Veillonella alcalescens in Mixed Continuous Cultures. Archs Oral Biol 1975, 20:407-410.
- [19]Rosan B, Lamont RJ: Dental plaque formation. Microbes Infect 2000, 2:1599-1607.
- [20]Scannapiece FA, Solomon L, Wadenya RO: Emergence in Human Dental Plaque and Host Distribution of Amylase-binding Streptococci. J Dent Res 1994, 73:1627-1635.
- [21]McNab R, Holmes AR, Clarke JM, Tannock GW, Jenkinson HF: Cell Surface Polypeptide CshA Mediates Binding of Streptococcus gordonii to Other Oral Bacteria and to Immobilized Fibronectin. Infect Immun 1996, 64:4204-4210.
- [22]Yajima A, Urano-Tashiro Y, Shimazu K, Takashima E, Takahashi Y, Konishi K: Hsa, an adhesin of Streptococcus gordonii DL1, binds to a2-3-linked sialic acid on glycophorin A of the erythrocyte membrane. Microbiol Immunol 2008, 52:69-77.
- [23]Maeda K, Nagata H, Yamamoto Y, Tanaka M, Tanaka J, Minamino N, Shizukuishi S: Glyceraldehyde-3-Phosphate Dehydrogenase of Streptococcus oralis Functions as a Coadhesin for Porphyromonas gingivalis Major Fimbriae. Infect Immun 2004, 72:1341-1348.
- [24]Park Y, James CE, Yoshimura F, Lamont RJ: Expression of the short fimbriae of Porphyromonas gingivalis is regulated in oral bacterial consortia. FEMS Microbiol Lett 2006, 262:65-71.
- [25]Frekkes P, Driessen AJM: Protein Targeting to the Bacterial Cytoplasmic Membrane. Microbiol Mol Biol Rev 1999, 63:161-173.
- [26]Moreno MS, Schneider BL, Maile RR, Weyler W, Saier MH Jr: Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 2001, 39:1366-1381.
- [27]Wen ZT, Burne RA: Functional Genomics Approach to Identifying Genes Required for Biofilm Development by Streptococcus mutans. Appl Environ Microbiol 2002, 68:1196-1203.
- [28]Kolenbrander PE, Andersen RN, Baker RA, Jenkinson HF: The Adhesion-Associated sca Operon in Streptococcus gordonii Encodes an Inducible High-Affinity ABC Transporter for Mn2+ Uptake. J Bact 1998, 180:290-295.
- [29]Andersen RN, Ganeshkumar N, Kolenbrander PE: Cloning of the Streptococcus gordonii PK488 Gene, Encoding an Adhesin Which Mediates Coaggregation with Actinomyces naeslundii PK606. Infect Immun 1993, 61:981-987.
- [30]Mascher T, Zahner D, Merai M, Balmelle N, de Saizieu AB, Hakenbeck R: The Streptococcus pneumoniae cia Regulon: CiaR Target Sites and Transcription Profile Analysis. J Bacteriol 2003, 185:60-70.
- [31]Darveau RP, Belton CM, Reife RA, Lamont RJ: Local Chemokine Paralysis, a Novel Pathogenic Mechanism for Porphyromonas gingivalis. Infect Immun 1998, 66:1660-1665.
- [32]Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, McIntosh ML, Alsam A, Kirkwood KL, Lambris JD, Darveau RP, Curtis MA: Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011, 10:497-506.
- [33]Bosch G, Skovran E, Xia Q, Wang T, Taub F, Miller JA, Lidstrom ME, Hackett M: Comprehensive proteomics of Methylobacterium extorquens AM1 metabolism under single carbon and nonmethylotrophic conditions. Proteomics 2008, 8:3494-3505.
- [34]Eng JK, McCormack AL, Yates JR: An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database. J American Soc Mass Spectrom 1994, 5:976-989.
- [35] : Porphyromonas gingivalis W83 Genome Page. [http://cmr.jcvi.org/tigr-scripts/CMR/GenomePage.cgi?org=gpg webcite]
- [36] : Streptococcus gordonii Challis NCTC7868 Genome Page. [http://cmr.jcvi.org/cgi-bin/CMR/GenomePage.cgi?org=gsg webcite]
- [37] : Fusobacterium nucleatum ATCC 25586 Genome Page. [http://cmr.jcvi.org/cgi-bin/CMR/GeneomePage.cgi?org=ntfn01 webcite]
- [38] : Mammalian Gene Collection. [http://mgc.nci.nih.gov webcite]
- [39]Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP: Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2003, 2:43-50.
- [40]Elias JE, Gibbons FD, King OD, Roth FP, Gygi SP: Intensity-based protein identification by machine learning from a library of tandem mass spectra. Nat Biotechnol 2004, 22:214-219.
- [41]Tabb DL, McDonald WH, Yates JR 3rd: DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 2002, 1:21-26.
- [42]Xia Q, Wang T, Park Y, Lamont RJ, Hackett M: Differential quantitative proteomics of Porphyromonas gingivalis by linear ion trap mass spectrometry: non-label methods comparison, q-values and LOWESS curve fitting. Int J Mass Spectrom 2007, 259:105-116.
- [43]Xia Q, Wang T, Taub F, Park Y, Capestany CA, Lamont RJ, Hackett M: Quantitative proteomics of intracellular Porphyromonas gingivalis. Proteomics 2007, 7:4323-4337.
- [44]Hendrickson EL, Xia Q, Wang T, Lamont RJ, Hackett M: Pathway analysis for intracellular Porphyromonas gingivalis using a strain ATCC 33277 specific database. BMC Microbiol 2009, 9:185. BioMed Central Full Text
- [45]Liu H, Sadygov RG, Yates JR 3rd: A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 2004, 76:4193-4201.
- [46]Sokal RR, Rohlf FJ: Biometry, the principles and practice of statistics in biological research. New York: WH Freeman; 1995:715-724.
- [47]Storey JD, Tibshirani R: Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 2003, 100:9440-9445.
- [48]Storey Research Group: Qvalue. [http://genomics.princeton.edu/storeylab/qvalue/ webcite]
- [49]Benjamini Y, Yekutieli D: Quantitative trait Loci analysis using the false discovery rate. Genetics 2005, 171:783-790.
- [50]da Huang W, Sherman BT, Tan Q, Kir J, Liu D, Bryant D, Guo Y, Stephens R, Baseler MW, Lane HC, et al.: DAVID Bioinformatics Resources: expanded annotation database and novel algorithms to better extract biology from large gene lists. Nucleic Acids Res 2007, 35:W169-W175.
PDF