Chapter 21 : Heterotypic Communities: Formation, Gene Regulation, and Development

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Heterotypic Communities: Formation, Gene Regulation, and Development, Page 1 of 2

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The composition of oral biofilm communities, and their pathogenic potential, may depend on interspecies binding and communication interactions. Multivalent coadhesive interactions characterize the binding of to oral streptococci such as and drive subsequent development of heterotypic - communities. Gene regulation by two-component systems (TCSs) is a common mechanism used by bacteria to modulate cell behavior in response to environmental changes. Following the initial binding interaction between and , adherent cells undergo a programmatic phenotypic shift in order to prepare for community living. produces autoinducer 2 (AI-2) and responds both to homologous signal and to AI-2 from other organisms such as and . The expression of GTF, Rgg, and exo-β;-D-fructosidase (fructanase) is downregulated in the absence of LuxS, whereas expression of tagatose 1,6-diphosphate aldolase is elevated. Contact with S. cristatus propagates a signal in P. gingivalis that causes downregulation of fimA expression. Signaling is mediated by arginine deiminase (ArcA) on the surface of . Biofilms tend to be polymicrobial in nature, and the subgingival plaque biofilm is an exemplar of this situation, with as many as 200 species present in any one individual.

Citation: Kuboniwa M, Lamont R. 2011. Heterotypic Communities: Formation, Gene Regulation, and Development, p 313-329. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch21

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Cellular Processes
Acidic Amino Acids
Aromatic Amino Acids
Basic Amino Acids
Acyl Coenzyme A
Cell Wall Biosynthesis
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Image of FIGURE 1

community- and biofilm-related gene cluster SGO_0275 to SGO_0307 (coordinates 292331 to 328700; 36.4 kb). Genes regulated in communities are number coded by putative community-related function. 1, transcriptional regulation and/or signaling; 2, capsule or cell wall biosynthesis; 3, protein folding and associated processing; 4, physiology.

Citation: Kuboniwa M, Lamont R. 2011. Heterotypic Communities: Formation, Gene Regulation, and Development, p 313-329. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch21
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Image of FIGURE 2

Role of Ltp1 in communities. Contact with transduces a signal (dashed arrow) that upregulates Ltp1 expression. Ltp1 downregulates (flat arrow) expression of exopolysaccharide and LuxS and upregulates (arrow) expression of the locus. Ltp1 also dephosphorylates Kgp. Phenotypic outcomes of Ltp1 activity include restricted biofilm development, reduced AI-2 signaling, increased uptake of hemin, and decreased cell-associated Kgp activity.

Citation: Kuboniwa M, Lamont R. 2011. Heterotypic Communities: Formation, Gene Regulation, and Development, p 313-329. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch21
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1. Aduse-Opoku, J.,, J. M. Slaney,, M. Rangarajan,, J. Muir,, K. A. Young, and, M. A. Curtis. 1997. The Tla protein of Porphyromonas gingivalis W50: a homolog of the RI protease precursor (PrpRI) is an outer membrane receptor required for growth on low levels of hemin. J. Bacteriol. 179:47784788.
2. Alamuri, P.,, and R. J. Maier. 2004. Methionine sulphoxide reductase is an important antioxidant enzyme in the gastric pathogen Helicobacter pylori. Mol. Microbiol. 53:13971406.
3. Amano, A.,, T. Fujiwara,, H. Nagata,, M. Kuboniwa,, A. Sharma,, H. T. Sojar,, R. J. Genco,, S. Hamada, and, S. Shizukuishi. 1997. Porphyromonas gingivalis fimbriae mediate coaggregation with Streptococcus oralis through specific domains. J. Dent. Res. 76:852857.
4. Arbibe, L.,, D. W. Kim,, E. Batsche,, T. Pedron,, B. Mateescu,, C. Muchardt,, C. Parsot, and, P. J. Sansonetti. 2007. An injected bacterial effector targets chromatin access for transcription factor NF-κB to alter transcription of host genes involved in immune responses. Nat. Immunol. 8:4756.
5. Ashiuchi, M.,, and H. Misono. 2002. Biochemistry and molecular genetics of poly-γ-glutamate synthesis. Appl. Microbiol. Biotechnol. 59:914.
6. Ashiuchi, M.,, C. Nawa,, T. Kamei,, J. J. Song,, S. P. Hong,, M. H. Sung,, K. Soda, and, H. Misono. 2001. Physiological and biochemical characteristics of poly gamma-glutamate synthetase complex of Bacillus subtilis. Eur. J. Biochem. 268:53215328.
7. Atack, J. M.,, and D. J. Kelly. 2008. Contribution of the stereospecific methionine sulphoxide reductases MsrA and MsrB to oxidative and nitrosative stress resistance in the food-borne pathogen Campylobacter jejuni. Microbiology 154:22192230.
8. Bach, H.,, K. G. Papavinasasundaram,, D. Wong,, Z. Hmama, and, Y. Av-Gay. 2008. Mycobacterium tuberculosis virulence is mediated by PtpA dephosphorylation of human vacuolar protein sorting 33B. Cell Host Microbe 3:316322.
9. Barnard, J. P.,, and M. W. Stinson. 1999. Influence of environmental conditions on hydrogen peroxide formation by Streptococcus gordonii. Infect. Immun. 67:65586564.
10. Basu, S.,, S. Pathak,, S. K. Pathak,, A. Bhattacharyya,, A. Banerjee,, M. Kundu, and, J. Basu. 2007. Mycobacterium avium-induced matrix metalloproteinase-9 expression occurs in a cyclooxygenase-2-dependent manner and involves phosphorylation- and acetylation-dependent chromatin modification. Cell. Microbiol. 9:28042816.
11. Battig, P.,, and K. Muhlemann. 2008. Influence of the spxB gene on competence in Streptococcus pneumoniae. J. Bacteriol. 190:11841189.
12. Bhagwat, S. P.,, J. Nary, and, R. A. Burne. 2001. Effects of mutating putative two-component systems on biofilm formation by Streptococcus mutans UA159. FEMS Microbiol. Lett. 205:225230.
13. Brooks, W.,, D. R. Demuth,, S. Gil, and, R. J. Lamont. 1997. Identification of a Streptococcus gordonii SspB domain that mediates adhesion to Porphyromonas gingivalis. Infect. Immun. 65:37533758.
14. Burne, R. A.,, and J. E. Penders. 1992. Characterization of the Streptococcus mutans GS-5 fruA gene encoding exo-β-D-fructosidase. Infect. Immun. 60:46214632.
15. Calfee, M. W.,, J. P. Coleman, and, E. C. Pesci. 2001. Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 98:1163311637.
16. Chung, W. O.,, Y. Park,, R. J. Lamont,, R. McNab,, B. Barbieri, and, D. R. Demuth. 2001. Signaling system in Porphyromonas gingivalis based on a LuxS protein. J. Bacteriol. 183:39033909.
17. Cook, G. S.,, J. W. Costerton, and, R. J. Lamont. 1998. Biofilm formation by Porphyromonas gingivalis and Streptococcus gordonii. J. Periodontal Res. 33:323327.
18. Cort, J. R.,, T. A. Ramelot,, D. Murray,, T. B. Acton,, L. C. Ma,, R. Xiao,, G. T. Montelione, and, M. A. Kennedy. 2008. Structure of an acetyl-CoA binding protein from Staphylococcus aureus representing a novel subfamily of GCN5-related N-acetyltransferase-like proteins. J. Struct. Funct. Genomics 9:720.
19. Daep, C. A.,, D. M. James,, R. J. Lamont, and, D. R. Demuth. 2006. Structural characterization of peptide-mediated inhibition of Porphyromonas gingivalis biofilm formation. Infect. Immun. 74:57565762.
20. Daep, C. A.,, R. J. Lamont, and, D. R. Demuth. 2008. Interaction of Porphyromonas gingivalis with oral streptococci requires a motif that resembles the eukaryotic nuclear receptor box protein-protein interaction domain. Infect. Immun. 76:32733280.
21. Dashper, S. G.,, C. A. Butler,, J. P. Lissel,, R. A. Paolini,, B. Hoffmann,, P. D. Veith,, N. M. O’Brien-Simpson,, S. L. Snelgrove,, J. T. Tsiros, and, E. C. Reynolds. 2005. A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J. Biol. Chem. 280:2809528102.
22. Dashper, S. G.,, A. Hendtlass,, N. Slakeski,, C. Jackson,, K. J. Cross,, L. Brownfield,, R. Hamilton,, I. Barr, and, E. C. Reynolds. 2000. Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis. J. Bacteriol. 182:64566462.
23. Demuth, D. R.,, Y. Duan,, W. Brooks,, A. R. Holmes,, R. McNab, and, H. F. Jenkinson. 1996. Tandem genes encode cell-surface polypeptides SspA and SspB which mediate adhesion of the oral bacterium Streptococcus gordonii to human and bacterial receptors. Mol. Microbiol. 20:403413.
24. Demuth, D. R.,, D. C. Irvine,, J. W. Costerton,, G. S. Cook, and, R. J. Lamont. 2001. Discrete protein determinant directs the species-specific adherence of Porphyromonas gingivalis to oral streptococci. Infect. Immun. 69:57365741.
25. Dhandayuthapani, S.,, M. W. Blaylock,, C. M. Bebear,, W. G. Rasmussen, and, J. B. Baseman. 2001. Peptide methionine sulfoxide reductase (MsrA) is a virulence determinant in Mycoplasma genitalium. J. Bacteriol. 183:56455650.
26. Diaz, P. I.,, N. I. Chalmers,, A. H. Rickard,, C. Kong,, C. L. Milburn,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72:28372848.
27. Dorel, C.,, O. Vidal,, C. Prigent-Combaret,, I. Vallet, and, P. Lejeune. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178:169175.
28. Douglas, T.,, D. S. Daniel,, B. K. Parida,, C. Jagannath, and, S. Dhandayuthapani. 2004. Methionine sulfoxide reductase A (MsrA) deficiency affects the survival of Mycobacterium smegmatis within macrophages. J. Bacteriol. 186:35903598.
29. Ezraty, B.,, L. Aussel, and, F. Barras. 2005. Methionine sulfoxide reductases in prokaryotes. Biochim. Biophys. Acta 1703:221229.
30. Federle, M. J.,, and B. L. Bassler. 2003. Interspecies communication in bacteria. J. Clin. Investig. 112:12911299.
31. Gardete, S.,, A. M. Ludovice,, R. G. Sobral,, S. R. Filipe,, H. de Lencastre, and, A. Tomasz. 2004. Role of murE in the expression of beta-lactam antibiotic resistance in Staphylococcus aureus. J. Bacteriol. 186:17051713.
32. Gill, S. R.,, D. E. Fouts,, G. L. Archer,, E. F. Mongodin,, R. T. Deboy,, J. Ravel,, I. T. Paulsen,, J. F. Kolonay,, L. Brinkac,, M. Beanan,, R. J. Dodson,, S. C. Daugherty,, R. Madupu,, S. V. Angiuoli,, A. S. Durkin,, D. H. Haft,, J. Vamathevan,, H. Khouri,, T. Utterback,, C. Lee,, G. Dimitrov,, L. Jiang,, H. Qin,, J. Weidman,, K. Tran,, K. Kang,, I. R. Hance,, K. E. Nelson, and, C. M. Fraser. 2005. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J. Bacteriol. 187:24262438.
33. Goulbourne, P. A.,, and R. P. Ellen. 1991. Evidence that Porphyromonas (Bacteroides) gingivalis fimbriae function in adhesion to Actinomyces viscosus. J. Bacteriol. 173:52665274.
34. Grangeasse, C.,, A. J. Cozzone,, J. Deutscher, and, I. Mijakovic. 2007. Tyrosine phosphorylation: an emerging regulatory device of bacterial physiology. Trends Biochem. Sci. 32:8694.
35. Grimaud, R.,, B. Ezraty,, J. K. Mitchell,, D. Lafitte,, C. Briand,, P. J. Derrick, and, F. Barras. 2001. Repair of oxidized proteins. Identification of a new methionine sulfoxide reductase. J. Biol. Chem. 276:4891548920.
36. Hardie, K. R.,, and K. Heurlier. 2008. Establishing bacterial communities by ‘word of mouth’: LuxS and autoinducer 2 in biofilm development. Nat. Rev. Microbiol. 6:635643.
37. Havarstein, L. S.,, P. Gaustad,, I. F. Nes, and, D. A. Morrison. 1996. Identification of the streptococcal competence-pheromone receptor. Mol. Microbiol. 21:863869.
38. He, Z.,, K. D. Stigers Lavoie,, P. A. Bartlett, and, M. D. Toney. 2004. Conservation of mechanism in three chorismate-utilizing enzymes. J. Am. Chem. Soc. 126:23782385.
39. Higuchi, M.,, Y. Yamamoto,, L. B. Poole,, M. Shimada,, Y. Sato,, N. Takahashi, and, Y. Kamio. 1999. Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. J. Bacteriol. 181:59405947.
40. Jagusztyn-Krynicka, E. K.,, J. B. Hansen,, V. L. Crow,, T. D. Thomas,, A. L. Honeyman, and, R. Curtiss III. 1992. Streptococcus mutans serotype c tagatose 6-phosphate pathway gene cluster. J. Bacteriol. 174:61526158.
41. James, C. E.,, Y. Hasegawa,, Y. Park,, V. Yeung,, G. D. Tribble,, M. Kuboniwa,, D. R. Demuth, and, R. J. Lamont. 2006. LuxS involvement in the regulation of genes coding for hemin and iron acquisition systems in Porphyromonas gingivalis. Infect. Immun. 74:38343844.
42. Jenkinson, H. F.,, and D. R. Demuth. 1997. Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol. Microbiol. 23:183190.
43. Keller, L.,, and M. G. Surette. 2006. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4:249258.
44. Kilic, A. O.,, L. Tao,, Y. Zhang,, Y. Lei,, A. Khammanivong, and, M. C. Herzberg. 2004. Involvement of Streptococcus gordonii β-glucoside metabolism systems in adhesion, biofilm formation, and in vivo gene expression. J. Bacteriol. 186:42464253.
45. Kimura, K.,, L. S. Tran,, I. Uchida, and, Y. Itoh. 2004. Characterization of Bacillus subtilis γ-glutamyltransferase and its involvement in the degradation of capsule poly-γ-glutamate. Microbiology 150:41154123.
46. Kocianova, S.,, C. Vuong,, Y. Yao,, J. M. Voyich,, E. R. Fischer,, F. R. DeLeo, and, M. Otto. 2005. Key role of poly-γ-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J. Clin. Investig. 115:688694.
47. Kolenbrander, P. E.,, R. N. Andersen,, D. S. Blehert,, P. G. Egland,, J. S. Foster, and, R. J. Palmer, Jr. 2002. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66:486505.
48. Kreth, J.,, Y. Zhang, and, M. C. Herzberg. 2008. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J. Bacteriol. 190:46324640.
49. Kuboniwa, M.,, G. D. Tribble,, C. E. James,, A. O. Kilic,, L. Tao,, M. C. Herzberg,, S. Shizukuishi, and, R. J. Lamont. 2006. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol. Microbiol. 60:121139.
50. Kuramitsu, H. K.,, X. He,, R. Lux,, M. H. Anderson, and, W. Shi. 2007. Interspecies interactions within oral microbial communities. Microbiol. Mol. Biol. Rev. 71:653670.
51. Lamont, R. J.,, C. A. Bevan,, S. Gil,, R. E. Persson, and, B. Rosan. 1993. Involvement of Porphyromonas gingivalis fimbriae in adherence to Streptococcus gordonii. Oral Microbiol. Immunol. 8:272276.
52. Lamont, R. J.,, A. El-Sabaeny,, Y. Park,, G. S. Cook,, J. W. Costerton, and, D. R. Demuth. 2002. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148:16271636.
53. Lee, J.,, A. Jayaraman, and, T. K. Wood. 2007. Indole is an interspecies biofilm signal mediated by SdiA. BMC Microbiol. 7:42.
54. Lee, W. L.,, B. Gold,, C. Darby,, N. Brot,, X. Jiang,, L. P. de Carvalho,, D. Wellner,, G. St. John,, W. R. Jacobs, Jr., and, C. Nathan. 2009. Mycobacterium tuberculosis expresses methionine sulphoxide reductases A and B that protect from killing by nitrite and hypochlorite. Mol. Microbiol. 71:583593.
55. Li, Y. H.,, P. C. Lau,, N. Tang,, G. Svensater,, R. P. Ellen, and, D. G. Cvitkovitch. 2002. Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans. J. Bacteriol. 184:63336342.
56. Lin, X.,, R. J. Lamont,, J. Wu, and, H. Xie. 2008. Role of differential expression of streptococcal arginine deiminase in inhibition of fimA expression in Porphyromonas gingivalis. J. Bacteriol. 190:43674371.
57. Loo, C. Y.,, D. A. Corliss, and, N. Ganesh-kumar. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182:13741382.
58. Lukat, G. S.,, W. R. McCleary,, A. M. Stock, and, J. B. Stock. 1992. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc. Natl. Acad. Sci USA 89:718722.
59. Lunsford, R. D. 1998. Streptococcal transformation: essential features and applications of a natural gene exchange system. Plasmid 39:1020.
60. Maeda, K.,, H. Nagata,, M. Kuboniwa,, K. Kataoka,, N. Nishida,, M. Tanaka, and, S. Shizukuishi. 2004. Characterization of binding of Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase to Porphyromonas gingivalis major fimbriae. Infect. Immun. 72:54755477.
61. Maeda, K.,, H. Nagata,, Y. Yamamoto,, M. Tanaka,, J. Tanaka,, N. Minamino, and, S. Shizukuishi. 2004. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus oralis functions as a coadhesin for Porphyromonas gingivalis major fimbriae. Infect. Immun. 72:13411348.
62. Maeda, K.,, G. D. Tribble,, C. M. Tucker,, C. Anaya,, S. Shizukuishi,, J. P. Lewis,, D. R. Demuth, and, R. J. Lamont. 2008. A Porphyromonas gingivalis tyrosine phosphatase is a multi-functional regulator of virulence attributes. Mol. Microbiol. 69:11531164.
63. Mayanagi, G.,, T. Sato,, H. Shimauchi, and, N. Takahashi. 2004. Detection frequency of periodontitis-associated bacteria by polymerase chain reaction in subgingival and supragingival plaque of periodontitis and healthy subjects. Oral Microbiol. Immunol. 19:379385.
64. McCleary, W. R.,, and J. B. Stock. 1994. Acetyl phosphate and the activation of two-component response regulators. J. Biol. Chem. 269:3156731572.
65. McNab, R.,, S. K. Ford,, A. El-Sabaeny,, B. Barbieri,, G. S. Cook, and, R. J. Lamont. 2003. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185:274284.
66. Merrick, M. 1988. Regulation of nitrogen assimilation by bacteria, p. 331–361. In J. Cole and, S. Ferguson (ed.), The Nitrogen and Sulfur Cycles. Cambridge University Press, Cambridge, United Kingdom.
67. Mintz, K. P.,, J. Moskovitz,, H. Wu, and, P. M. Fives-Taylor. 2002. Peptide methionine sulfoxide reductase (MsrA) is not a major virulence determinant for the oral pathogen Actino-bacillus actinomycetemcomitans. Microbiology 148:36953703.
68. Moskovitz, J.,, V. K. Singh,, J. Requena,, B. J. Wilkinson,, R. K. Jayaswal, and, E. R. Stadtman. 2002. Purification and characterization of methionine sulfoxide reductases from mouse and Staphylococcus aureus and their substrate stereospecificity. Biochem. Biophys. Res. Commun. 290:6265.
69. Musumeci, L.,, C. Bongiorni,, L. Tautz,, R. A. Edwards,, A. Osterman,, M. Perego,, T. Mustelin, and, N. Bottini. 2005. Low-molecular-weight protein tyrosine phosphatases of Bacillus subtilis. J. Bacteriol. 187:49454956.
70. Nadell, C. D.,, J. B. Xavier,, S. A. Levin, and, K. R. Foster. 2008. The evolution of quorum sensing in bacterial biofilms. PLoS Biol. 6:e14.
71. Nagy, Z.,, and L. Tora. 2007. Distinct GCN5/PCAF-containing complexes function as coactivators and are involved in transcription factor and global histone acetylation. Oncogene 26:53415357.
72. Olczak, T.,, W. Simpson,, X. Liu, and, C. A. Genco. 2005. Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiol. Rev. 29:119144.
73. Otto, K.,, and T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99:22872292.
74. Pagliarulo, C.,, P. Salvatore,, L. R. De Vitis,, R. Colicchio,, C. Monaco,, M. Tredici,, A. Tala,, M. Bardaro,, A. Lavitola,, C. B. Bruni, and, P. Alifano. 2004. Regulation and differential expression of gdhA encoding NADP-specific glutamate dehydrogenase in Neisseria meningitidis clinical isolates. Mol. Microbiol. 51:17571772.
75. Paramonov, N.,, M. Rangarajan,, A. Hashim,, A. Gallagher,, J. Aduse-Opoku,, J. M. Slaney,, E. Hounsell, and, M. A. Curtis. 2005. Structural analysis of a novel anionic polysaccharide from Porphyromonas gingivalis strain W50 related to Arg-gingipain glycans. Mol. Microbiol. 58:847863.
76. Parkins, M. D.,, H. Ceri, and, D. G. Storey. 2001. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol. Microbiol. 40:12151226.
77. Pericone, C. D.,, D. Bae,, M. Shchepetov,, T. McCool, and, J. N. Weiser. 2002. Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae. J. Bacteriol. 184:43924399.
78. Pericone, C. D.,, S. Park,, J. A. Imlay, and, J. N. Weiser. 2003. Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J. Bacteriol. 185:68156825.
79. Preneta, R.,, S. Jarraud,, C. Vincent,, P. Doublet,, B. Duclos,, J. Etienne, and, A. J. Cozzone. 2002. Isolation and characterization of a protein-tyrosine kinase and a phosphotyrosine-protein phosphatase from Klebsiella pneumoniae. Comp. Biochem. Physiol. B 131:103112.
80. Prigent-Combaret, C.,, O. Vidal,, C. Dorel, and, P. Lejeune. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181:59936002.
81. Quirynen, M.,, R. Vogels,, M. Pauwels,, A. D. Haffajee,, S. S. Socransky,, N. G. Uzel, and, D. van Steenberghe. 2005. Initial subgingival colonization of ‘pristine’ pockets. J. Dent. Res. 84:340344.
82. Rainey, P. B.,, and K. Rainey. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425:7274.
83. Roggiani, M.,, and D. Dubnau. 1993. ComA, a phosphorylated response regulator protein of Bacillus subtilis, binds to the promoter region of srfA. J. Bacteriol. 175:31823187.
84. Savkur, R. S.,, and T. P. Burris. 2004. The coactivator LXXLL nuclear receptor recognition motif. J. Pept. Res. 63:207212.
85. Schembri, M. A.,, K. Kjaergaard, and, P. Klemm. 2003. Global gene expression in Escherichia coli biofilms. Mol. Microbiol. 48:253267.
86. Shemesh, M.,, A. Tam, and, D. Steinberg. 2007. Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology 153:13071317.
87. Simionato, M. R.,, C. M. Tucker,, M. Kuboniwa,, G. Lamont,, D. R. Demuth,, G. D. Tribble, and, R. J. Lamont. 2006. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74:64196428.
88. Simpson, W.,, T. Olczak, and, C. A. Genco. 2000. Characterization and expression of HmuR, a TonB-dependent hemoglobin receptor of Porphyromonas gingivalis. J. Bacteriol. 182:57375748.
89. Slots, J.,, and R. J. Gibbons. 1978. Attachment of Bacteroides melaninogenicus subsp. asaccharolyticus to oral surfaces and its possible role in colonization of the mouth and of periodontal pockets. Infect. Immun. 19:254264.
90. Smith, E. I.,, B. Austen,, K. Blumenthal, and, J. Nyc. 1975. Glutamate dehydrogenases, p. 294–352. In P. Boyer (ed.), The Enzymes, vol. XI. Academic Press, New York, NY.
91. Socransky, S. S.,, and A. D. Haffajee. 2005. Periodontal microbial ecology. Periodontol. 2000 38:135187.
92. Socransky, S. S.,, A. D. Haffajee,, L. A. Ximenez-Fyvie,, M. Feres, and, D. Mager. 1999. Ecological considerations in the treatment of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis periodontal infections. Periodontol. 2000 20:341362.
93. Spellerberg, B.,, D. R. Cundell,, J. Sandros,, B. J. Pearce,, I. Idanpaan-Heikkila,, C. Rosenow, and, H. R. Masure. 1996. Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae. Mol. Microbiol. 19:803813.
94. Stanley, N. R.,, and B. A. Lazazzera. 2005. Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-γ-DL-glutamic acid production and biofilm formation. Mol. Microbiol. 57:11431158.
95. St. John, G.,, N. Brot,, J. Ruan,, H. Erdjument-Bromage,, P. Tempst,, H. Weissbach, and, C. Nathan. 2001. Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc. Natl. Acad. Sci. USA 98:99019906.
96. Stock, A. M.,, V. L. Robinson, and, P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183215.
97. Storz, G.,, and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188194.
98. Sulavik, M. C.,, G. Tardif, and, D. B. Clewell. 1992. Identification of a gene, rgg, which regulates expression of glucosyltransferase and influences the Spp phenotype of Streptococcus gordonii Challis. J. Bacteriol. 174:35773586.
99. Syn, C. K.,, J. K. Magnuson,, M. T. Kingsley, and, S. Swarup. 2004. Characterization of Pseudomonas putida genes responsive to nutrient limitation. Microbiology 150:16611669.
100. Takazoe, I.,, T. Nakamura, and, K. Okuda. 1984. Colonization of the subgingival area by Bacteroides gingivalis. J. Dent. Res. 63:422426.
101. Tanaka, S.,, M. Minami,, Y. Murakami,, T. Ogiwara,, K. Seto,, M. Shoji,, A. Hirata,, S. Abe,, S. Watanabe, and, S. Fujisawa. 2006. The detection of Porphyromonas gingivalis, Prevotella intermedia and Actinobacillus actinomycetemcomitans in tooth, tongue and buccal mucosa plaques in children, using immunoslot blot assay (IBA). J. Clin. Pediatr. Dent. 30:251256.
102. Tanaka, S.,, Y. Murakami,, K. Seto,, K. Takamori,, M. Yosida,, K. Ochiai,, S. Watanabe, and, S. Fujisawa. 2003. The detection of Porphyromonas gingivalis, Prevotella intermedia, and Actinobacillus actinomycetemcomitans in the supragingival plaque of children with and without caries. Pediatr. Dent. 25:143148.
103. Tanner, A. C.,, P. M. Milgrom,, R. Kent, Jr.,, S. A. Mokeem,, R. C. Page,, C. A. Riedy,, P. Weinstein, and, J. Bruss. 2002. The microbiota of young children from tooth and tongue samples. J. Dent. Res. 81:5357.
104. Tavender, T. J.,, N. M. Halliday,, K. R. Hardie, and, K. Winzer. 2008. LuxS-independent formation of AI-2 from ribulose-5-phosphate. BMC Microbiol. 8:98.
105. Tezal, M.,, F. A. Scannapieco,, J. Wactawski-Wende,, S. G. Grossi, and, R. J. Genco. 2006. Supragingival plaque may modify the effects of subgingival bacteria on attachment loss. J. Periodontol. 77:808813.
106. Toledo-Arana, A.,, N. Merino,, M. Vergara-Irigaray,, M. Debarbouille,, J. R. Penades, and, I. Lasa. 2005. Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J. Bacteriol. 187:53185329.
107. Tran, L. S.,, T. Nagai, and, Y. Itoh. 2000. Divergent structure of the ComQXPA quorumsensing components: molecular basis of strain-specific communication mechanism in Bacillus subtilis. Mol. Microbiol. 37:11591171.
108. Troy, F. A. 1973. Chemistry and biosynthesis of the poly(γ-D-glutamyl) capsule in Bacillus licheniformis. I. Properties of the membranemediated biosynthetic reaction. J. Biol. Chem. 248:305315.
109. Van Winkelhoff, A. J.,, and K. Boutaga. 2005. Transmission of periodontal bacteria and models of infection. J. Clin. Periodontol. 32(Suppl. 6):1627.
110. Vattanaviboon, P.,, C. Seeanukun,, W. Whangsuk,, S. Utamapongchai, and, S. Mongkolsuk. 2005. Important role for methionine sulfoxide reductase in the oxidative stress response of Xanthomonas campestris pv. phaseoli. J. Bacteriol. 187:58315836.
111. Vendeville, A.,, K. Winzer,, K. Heurlier,, C. M. Tang, and, K. R. Hardie. 2005. Making “sense” of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3:383396.
112. Vetting, M. W.,, L. P. S. de Carvalho,, M. Yu,, S. S. Hegde,, S. Magnet,, S. L. Roderick, and, J. S. Blanchard. 2005. Structure and functions of the GNAT superfamily of acetyltransferases. Arch. Biochem. Biophys. 433:212226.
113. Vriesema, A. J.,, J. Dankert, and, S. A. Zaat. 2000. A shift from oral to blood pH is a stimulus for adaptive gene expression of Streptococcus gordonii CH1 and induces protection against oxidative stress and enhanced bacterial growth by expression of msrA. Infect. Immun. 68:10611068.
114. Walter, J.,, P. Chagnaud,, G. W. Tannock,, D. M. Loach,, F. Dal Bello,, H. F. Jenkinson,, W. P. Hammes, and, C. Hertel. 2005. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl. Environ. Microbiol. 71:979986.
115. Wanner, B. L. 1993. Gene regulation by phosphate in enteric bacteria. J. Cell. Biochem. 51:4754.
116. Wei, K.,, D. J. Tang,, Y. Q. He,, J. X. Feng,, B. L. Jiang,, G. T. Lu,, B. Chen, and, J. L. Tang. 2007. hpaR, a putative marR family transcriptional regulator, is positively controlled by HrpG and HrpX and involved in the pathogenesis, hypersensitive response, and extracellular protease production of Xanthomonas campestris pathovar campestris. J. Bacteriol. 189:20552062.
117. Weissbach, H.,, L. Resnick, and, N. Brot. 2005. Methionine sulfoxide reductases: history and cellular role in protecting against oxidative damage. Biochim. Biophys. Acta 1703:203212.
118. Whiteley, M.,, M. G. Bangera,, R. E. Bumgarner,, M. R. Parsek,, G. M. Teitzel,, S. Lory, and, E. P. Greenberg. 2001. Gene expression in Pseudomonas aeruginosa biofilms. Nature 413:860864.
119. Wizemann, T. M.,, J. Moskovitz,, B. J. Pearce,, D. Cundell,, C. G. Arvidson,, M. So,, H. Weissbach,, N. Brot, and, H. R. Masure. 1996. Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens. Proc. Natl. Acad. Sci. USA 93:79857990.
120. Xavier, J. B.,, and K. R. Foster. 2007. Cooperation and conflict in microbial biofilms. Proc. Natl. Acad. Sci. USA 104:876881.
121. Xavier, K. B.,, and B. L. Bassler. 2003. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol. 6:191197.
122. Xie, H.,, G. S. Cook,, J. W. Costerton,, G. Bruce,, T. M. Rose, and, R. J. Lamont. 2000. Intergeneric communication in dental plaque biofilms. J. Bacteriol. 182:70677069.
123. Xie, H.,, N. Kozlova, and, R. J. Lamont. 2004. Porphyromonas gingivalis genes involved in fimA regulation. Infect. Immun. 72:651658.
124. Xie, H.,, X. Lin,, B. Y. Wang,, J. Wu, and, R. J. Lamont. 2007. Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153:32283234.
125. Ximenez-Fyvie, L. A.,, A. D. Haffajee, and, S. S. Socransky. 2000. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J. Clin. Periodontol. 27:648657.
126. Ximenez-Fyvie, L. A.,, A. D. Haffajee, and, S. S. Socransky. 2000. Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J. Clin. Periodontol. 27:722732.
127. Yang, E. Y.,, A. C. Tanner,, P. Milgrom,, S. A. Mokeem,, C. A. Riedy,, A. T. Spadafora,, R. C. Page, and, J. Bruss. 2002. Periodontal pathogen detection in gingiva/tooth and tongue flora samples from 18- to 48-month-old children and periodontal status of their mothers. Oral Microbiol. Immunol. 17:5559.
128. Yoshida, Y.,, T. Sasaki,, S. Ito,, H. Tamura,, K. Kunimatsu, and, H. Kato. 2009. Identification and molecular characterization of tryptophanase encoded by tnaA in Porphyromonas gingivalis. Microbiology 155:968978.
129. Zhang, Y.,, Y. Lei,, A. Khammanivong, and, M. C. Herzberg. 2004. Identification of a novel two-component system in Streptococcus gordonii V288 involved in biofilm formation. Infect. Immun. 72:34893494.
130. Zhang, Y.,, M. Whiteley,, J. Kreth,, Y. Lei,, A. Khammanivong,, J. N. Evavold,, J. Fan, and, M. C. Herzberg. 2009. The two-component system BfrAB regulates expression of ABC transporters in Streptococcus gordonii and Streptococcus sanguinis. Microbiology 155:165173.


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Blast analysis of streptococcal and related species genome sequences with BAR sequence

Citation: Kuboniwa M, Lamont R. 2011. Heterotypic Communities: Formation, Gene Regulation, and Development, p 313-329. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch21
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genes required for community development with cells

Citation: Kuboniwa M, Lamont R. 2011. Heterotypic Communities: Formation, Gene Regulation, and Development, p 313-329. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch21

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