Intercellular communications in multispecies oral microbial communities

Frontiers in Microbiology

Volumn 5, Issue JULY, 2014, Pages

  Guo, Lihong ^a   He, Xuesong ^a   Shi, Wenyuan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cell cell communication; Coadhesion; Metabolic interactions; Oral microbial community; Signaling transduction

Indexed keywords

BIOFILM; CELL COMMUNICATION; CONFOCAL MICROSCOPY; ENZYME ACTIVITY; GENE EXPRESSION; MICROBIAL COMMUNITY; MOUTH CAVITY; NONHUMAN; OXYGEN TENSION; QUORUM SENSING; REVIEW; SIGNAL TRANSDUCTION; STREPTOCOCCUS MUTANS; TUMOR MICROENVIRONMENT;

EID: 84905375528     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00328     Document Type: Review

References (170)

1. Abe, T., Murakami, Y., Nagano, K., Hasegawa, Y., Moriguchi, K., Ohno, N.,et al. (2011). OmpA-like.protein influences cell shape and adhesive activity of Tannerella forsythia. Mol. Oral Microbiol. 26, 374-387. doi: 10.1111/j.2041-1014.2011.00625.x
2. Arevalo-Ferro, C., Hentzer, M., Reil, G., Görg, A., Kjelleberg, S., Givskov, M.,et al. (2003). Identification of quorumsensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5, 1350-1369. doi: 10.1046/j.1462-2920.2003.00532.x
3. Avila, M., Ojcius, D. M., and Yilmaz, ö. (2009). The oral microbiota: living with a permanent guest. DNA Cell Biol. 28, 405-411. doi: 10.1089/dna.2009.0874
4. Bamford, C. V., d'Mello, A., Nobbs, A. H., Dutton, L. C., Vickerman, M. M., and Jenkinson, H. F. (2009). Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 77, 3696-3704. doi: 10.1128/IAI.00438-09
5. Barnes, A. M., Ballering, K. S., Leibman, R. S., Wells, C. L., and Dunny, G. M. (2012). Enterococcus faecalis produces abundant extracellular structures containing DNA in the absence of cell lysis during early biofilm formation. MBio 3, e00193-e00212. doi: 10.1128/mBio.00193-12
6. Bassler, B. L., Greenberg, E. P., and Stevens, A. M. (1997). Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol. 179, 4043-4045.
7. Biyikoglu, B., Ricker, A., and Diaz, P. I. (2012). Strain-specific colonization patterns and serum modulation of multi-species oral biofilm development. Anaerobe 18, 459-470. doi: 10.1016/j.anaerobe.2012.06.003
8. Bowen, W. H., and Koo, H. (2011). Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 45, 69-86. doi: 10.1159/000324598
9. Bradshaw, D. J., and Marsh, P. D. (1998). Analysis of pH-driven disruption of oral microbial communities in vitro. Caries Res. 32, 456-462. doi: 10.1159/000016487
10. Bradshaw, D. J., Marsh, P. D., Watson, G. K., and Allison, C. (1998). Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect. Immun. 66, 4729-4732.
11. Brooks, W., Demuth, D. R., Gil, S., and Lamont, R. J. (1997). Identification of a Streptococcus gordonii SspB domain that mediates adhesion to Porphyromonas gingivalis. Infect. Immun. 65, 3753-3758.
12. Brown, S. A., and Whiteley, M. (2007). A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J. Bacteriol. 189, 6407-6414. doi: 10.1128/JB.00554-07
13. Capestany, C. A., Kuboniwa, M., Jung, I. Y., Park, Y., Tribble, G. D., and Lamont, R. J. (2006). Role of the Porphyromonas gingivalis InlJ protein in homotypic and heterotypic biofilm development. Infect. Immun. 74, 3002-3005. doi: 10.1128/IAI.74.5.3002-3005.2006
14. Caufield, P. W., Dasanayake, A. P., Li, Y., Pan, Y., Hsu, J., and Hardin, J. M. (2000). Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect. Immun. 68, 4018-4023. doi: 10.1128/IAI.68.7.4018-4023.2000
15. Chalmers, N. I., Palmer, R. J., Cisar, J. O., and Kolenbrander, P. E. (2008). Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J. Bacteriol. 190, 8145-8154. doi: 10.1128/JB.00983-08
16. Chalmers, N. I., Palmer, R. J. Jr., Du-Thumm, L., Sullivan, R., Shi, W., and Kolenbrander, P. E. (2007). Use of quantum dot luminescent probes to achieve single-cell resolution of human oral bacteria in biofilms. Appl. Environ. Microbiol. 73, 630-636. doi: 10.1128/AEM.02164-06
17. Chawla, A., Hirano, T., Bainbridge, B. W., Demuth, D. R., Xie, H., and Lamont, R. J. (2010). Community signaling between Streptococcus gordonii and Porphyromonas gingivalis is controlled by the transcriptional regulator CdhR. Mol. Microbiol. 78, 1510-1522. doi: 10.1111/j.1365-2958.2010.07420.x
18. Christopher, A. B., Arndt, A., Cugini, C., and Davey, M. E. (2010). A streptococcal effector protein that inhibits Porphyromonas gingivalis biofilm development. Microbiology 156, 3469-3477. doi: 10.1099/mic.0.042671-0
19. Chung, W. O., Park, Y., Lamont, R. J., McNab, R., Barbieri, B., and Demuth, D. R. (2001). Signaling system in Porphyromonas gingivalis based on a LuxS protein. J. Bacteriol. 183, 3903-3909. doi: 10.1128/JB.183.13.3903-3909.2001
20. Cisar, J. O., Kolenbrander, P. E., and McIntire, F. C. (1979). Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect. Immun. 24, 742-752.
21. Cogoni, V., Morgan-Smith, A., Fenno, J. C., Jenkinson, H. F., and Dymock, D. (2012). Treponema denticola chymotrypsin-like proteinase (CTLP) integrates spirochaetes within oral microbial communities. Microbiology 158, 759-770. doi: 10.1099/mic.0.055939-0
22. Cruz, M. R., Graham, C. E., Gagliano, B. C., Lorenz, M. C., and Garsin, D. A. (2013). Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect. Immun. 81, 189-200. doi: 10.1128/IAI.00914-12
23. Cuadra-Saenz, G., Rao, D. L., Underwood, A. J., Belapure, S. A., Campagna, S. R., Sun, Z.,et al. (2012). Autoinducer-2 influences interactions amongst pioneer colonizing streptococci in oral biofilms. Microbiology 158, 1783-1795. doi: 10.1099/mic.0.057182-0
24. Curtis, M. A., Hawley, S. A., and Aduse-Opoku, J. (1999). The rag locus of Porphyromonas gingivalis: a novel pathogenicity island. J. Periodontol. Res. 34, 400-440. doi: 10.1111/j.1600-0765.1999.tb02273.x
25. Cvitkovitch, D. G. (2001). Genetic competence and transformation in oral streptococci. Crit. Rev. Oral Biol. Med. 12, 217-243. doi: 10.1177/10454411010120030201
26. Daep, C. A., Novak, E. A., Lamont, R. J., and Demuth, D. R. (2011). Structural dissection and in vivo effectiveness of a peptide inhibitor of Porphyromonas gingivalis adherence to Streptococcus gordonii. Infect. Immun. 79, 67-74. doi: 10.1128/IAI.00361-10
27. Demuth, D. R., Duan, Y., Brooks, W., Holmes, A. R., McNab, R., and Jenkinson, H. F. (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, 403-413. doi: 10.1111/j.1365-2958.1996.tb02627.x
28. Demuth, D. R., Irvine, D. C., Costerton, J. W., Cook, G. S., and Lamont, R. J. (2001). Discrete protein determinant directs the species-specific adherence of Porphyromonas gingivalis to oral streptococci. Infect. Immun. 69, 5736-5741. doi: 10.1128/IAI.69.9.5736-5741.2001
29. Deng, D. M., Liu, M. J., ten Cate, J. M., and Crielaard, W. (2007). The VicRK system of Streptococcus mutans responds to oxidative stress. J. Dent. Res. 86, 606-610. doi: 10.1177/154405910708600705
30. Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C. R., Yu, W. H.,et al. (2010). The human oral microbiome. J. Bacteriol. 192, 5002-5017. doi: 10.1128/JB.00542-10
31. Diaz, P. I., Zilm, P. S., and Rogers, A. H. (2002). Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbondioxide-depleted environments. Microbiology 148, 467-472.
32. Dige, I., Raarup, M. K., Nyengaard, J. R., Kilian, M., and Nyvad, B. (2009). Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155, 2116-2126. doi: 10.1099/mic.0.027706-0
33. Ding, A. M., Palmer, R. J. Jr., Cisar, J. O., and Kolenbrander, P. E. (2010). Shear-enhanced oral microbial adhesion. Appl. Environ. Microbiol. 76, 1294-1297. doi: 10.1128/AEM.02083-09
34. Dû, L. D., and Kolenbrander, P. E. (2000). Identification of saliva-regulated genes of Streptococcus gordonii DL1 by differential display using random arbitrarily primed PCR. Infect. Immun. 68, 4834-4837. doi: 10.1128/IAI.68.8.4834-4837.2000
35. Dunman, P. M., Murphy, E., Haney, S., Palacios, D., Tucker-Kellogg, G., Wu, S.,et al. (2001). Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/ or sarA loci. J. Bacteriol. 183, 7341-7353. doi: 10.1128/JB.183.24.7341-7353.2001
36. Egland, P. G., Palmer, R. J., and Kolenbrander, P. E. (2004). Interspecies communication in Streptococcus gordonii-Veillonella atypicabiofilms: signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. U.S.A. 101, 16917-16922. doi: 10.1073/pnas.0407457101
37. Fong, K. P., Chung, W. O., Lamont, R. J., and Demuth, D. R. (2001). Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect. Immun. 69, 7625-7634. doi: 10.1128/IAI.69.12.7625-7634.2001
38. Frias, J., Olle, E., and Alsina, M. (2001). Periodontal pathogens produce quorum sensing signal molecules. Infect. Immun. 69, 3431-3434. doi: 10.1128/IAI.69.5.3431-3434.2001
39. Fujishima, K., Kawada-Matsuo, M., Oogai, Y., Tokuda, M., Torii, M., and Komatsuzawa, H. (2013). dpr and sod in Streptococcus mutans are involved in coexistence with S. sanguinis, and PerR is associated with resistance to H2O2. Appl. Environ. Microbiol. 79, 1436-1443. doi: 10.1128/AEM.03306-12
40. Gong, Y., Tian, X. L., Sutherland, T., Sisson, G., Mai, J., Ling, J.,et al. (2009). Global transcriptional analysis of acid-inducible genes in Streptococcus mutans: multiple two-component systems involved in acid adaptation. Microbiology 155, 3322-3332. doi: 10.1099/mic.0.031591-0
41. Gregoire, S., Xiao, J., Silva, B. B., Gonzalez, I., Agidi, P. S., Klein, M. I.,et al. (2011). Role of glucosyltransferase B in interactions of Candida albicans with Streptococcus mutans and with an experimental pellicle on hydroxyapatite surfaces. Appl. Environ. Microbiol. 77, 6357-6367. doi: 10.1128/AEM.05203-11
42. Grenier, D. (1992). Nutritional interactions between two suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis. Infect. Immun. 60, 5298-5301.
43. Hamada, T., Kawashima, M., Watanabe, H., Tagami, J., and Senpuku, H. (2004). Molecular interactions of surface protein peptides of Streptococcus gordonii with human salivary components. Infect. Immun. 72, 4819-4826. doi: 10.1128/IAI.72.8.4819-4826.2004
44. Hardie, K. R., and Heurlier, K. (2008). Establishing bacterial communities by "word of mouth": LuxS and autoinducer 2 in biofilm development. Nat. Rev. Microbiol. 6, 635-643. doi: 10.1038/nrmicro1916
45. Håvarstein, L. S., Hakenbeck, R., and Gaustad, P. (1997). Natural competence in the genus Streptococcus: evidence that streptococci can change pherotype by interspecies recombinational exchanges. J. Bacteriol. 179, 6589-6594.
46. He, X., Hu, W., Kaplan, C. W., Guo, L., Shi, W., and Lux, R. (2012). Adherence to streptococci facilitates Fusobacterium nucleatum integration into an oral microbial community. Microb. Ecol. 63, 532-542. doi: 10.1007/s00248-011-9989-2
47. Hendrickson, E. L., Wang, T., Dickinson, B. C., Whitmore, S. E., Wright, C. J., Lamont, R. J.,et al. (2012). Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiol. 12:211. doi: 10.1186/1471-2180-12-211
48. Heng, N. C. K., Tagg, J. R., and Tompkins, G. R. (2007). Competence-dependent bacteriocin production by Streptococcus gordonii DL1 (Challis). J. Bacteriol. 189, 1468-1472. doi: 10.1128/JB.01174-06
49. Hillman, J. D., Socransky, S. S., and Shivers, M. (1985). The relationships between streptococcal species and periodontopathic bacteria in human dental plaque. Arch. Oral Biol. 30, 791-795. doi: 10.1016/0003-9969(85)90133-5
50. Hojo, K., Nagaoka, S., Ohshima, T., and Maeda, N. (2009). Bacterial interactions in dental biofilm development. J. Dent. Res. 88, 982-990. doi: 10.1177/0022034509346811
51. Huber, B., Riedel, K., Hentzer, M., Heydorn, A., Gotschlich, A., Givskov, M.,et al. (2001). The cep quorumsensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147, 2517-2528.
52. Ikegami, A., Honma, K., Sharma, A., and Kuramitsu, H. K. (2004). Multiple functions of the leucine-rich repeat protein LrrA of Treponema denticola. Infect. Immun. 72, 4619-4627. doi: 10.1128/IAI.72.8.4619-4627.2004
53. Inagaki, S., Kuramitsu, H. K., and Sharma, A. (2005). Contact-dependent regulation of a Tannerella forsythia virulence factor, BspA, in biofilms. FEMS Microbiol. Lett. 249, 291-296. doi: 10.1016/j.femsle.2005.06.032
54. Ishihara, K., Nabuchi, A., Ito, R., Miyachi, K., Kuramitsu, H. K., and Okuda, K. (2004). Correlation between detection rates of periodontopathic bacterial DNA in carotid coronary stenotic artery plaque and in dental plaque samples. J. Clin. Microbiol. 42, 1313-1315. doi: 10.1128/JCM.42.3.1313-1315.2004
55. Jakubovics, N. S., Gill, S. R., Iobst, S. E., Vickerman, M. M., and Kolenbrander, P. E. (2008a). Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J. Bacteriol. 190, 3646-3657. doi: 10.1128/JB.00088-08
56. Jakubovics, N. S., Gill, S. R., Vickerman, M. M., and Kolenbrander, P. E. (2008b). Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. FEMS Microbiol. Ecol. 66, 637-644. doi: 10.1111/j.1574-6941.2008.00585.x
57. James, C. E., Hasegawa, Y., Park, Y., Yeung, V., Tribble, G. D., Kuboniwa, M.,et al. (2006). LuxS involvement in the regulation of genes coding for hemin and iron acquisition systems in Porphyromonas gingivalis. Infect. Immun. 74, 3834-3844. doi: 10.1128/IAI.01768-05
58. Jang, Y. J., Choi, Y. J., Lee, S. H., Jun, H. K., and Choi, B. K. (2013a). Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Arch. Oral Biol. 58, 17-27. doi: 10.1016/j.archoralbio.2012.04.016
59. Jang, Y. J., Sim, J., Jun, H. K., and Choi, B. K. (2013b). Differential effect of autoinducer 2 of Fusobacterium nucleatum on oral streptococci. Arch. Oral Biol. 58, 1594-1602. doi: 10.1016/j.archoralbio.2013.08.006
60. Jarosz, L. M., Deng, D. M., van der Mei, H. C., Crielaard, W., and Krom, B. P. (2009). Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot. Cell 8, 1658-1664. doi: 10.1128/EC.00070-09
61. Jayaraman, A., and Wood, T. K. (2008). Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu. Rev. Biomed. Eng. 10, 145-167. doi: 10.1146/annurev.bioeng.10.061807.160536
62. Jenkinson, H. F., and Lamont, R. J. (2005). Oral microbial communities in sickness and in health. Trends Microbiol. 13, 589-595. doi: 10.1016/j.tim.2005.09.006
63. Johnson, B. P., Jensen, B. J., Ransom, E. M., Heinemann, K. A., Vannatta, K. M., Egland, K. A.,et al. (2009). Interspecies signaling between Veillonella atypica and Streptococcus gordonii requires the transcription factor CcpA. J. Bacteriol. 191, 5563-5565. doi: 10.1128/JB.01226-08
64. Kaewsrichan, J., Douglas, C. W. I., Nissen-Meyer, J., Fimland, G., and Teanpaisan, R. (2004). Characterization of a bacteriocin produced by Prevotella nigrescens ATCC 25261. Lett. Appl. Microbiol. 39, 451-458. doi: 10.1111/j.1472-765X.2004.01608.x
65. Kaplan, C. W., Lux, R., Haake, S. K., and Shi, W. (2009). The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol. 71, 35-47. doi: 10.1111/j.1365-2958.2008.06503.x
66. Kaplan, J. B., Ragunath, C., Ramasubbu, N., and Fine, D. H. (2003). Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J. Bacteriol. 185, 4693-4698. doi: 10.1128/JB.185.16.4693-4698.2003
67. Kerr, J. E., Abramian, J. R., Dao, D. H., Rigney, T. W., Fritz, J., Pham, T.,et al. (2014). Genetic exchange of fimbrial alleles exemplifies the adaptive virulence strategy of Porphyromonas gingivalis. PLoS ONE 13:e91696. doi: 10.1371/journal.pone.0091696
68. Kolenbrander, P. E. (2011). Multispecies communities: interspecies interactions influence growth on saliva as sole nutritional source. Int. J. Oral 3, 49-54. doi: 10.4248/IJOS11025
69. Kolenbrander, P. E., Andersen, R. N., Baker, R. A., Jenkinson, H. F. (1998a). The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J. Bacteriol. 180, 290-295.
70. Kolenbrander, P. E., Andersen, R. N., and Moore, L. V. (1998b). Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect. Immun. 57, 3194-3203.
71. Kolenbrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S., and Palmer, R. J. Jr. (2002). Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66, 486-505. doi: 10.1128/MMBR.66.3.486-505.2002
72. Kolenbrander, P. E., Andersen, R. N., and Ganeshkumar, N. (1994). Nucleotide sequence of the Streptococcus gordonii PK488 coaggregation adhesin gene, scaA, and ATP-binding cassette. Infect. Immun. 62, 4469-4480.
73. Kolenbrander, P. E., Palmer, R. J. Jr., Periasamy, S., and Jakubovics, N. S. (2010). Oral multispecies biofilm development and the key role of cell-cell distance. Nat. Rev. Microbiol. 8, 471-480. doi: 10.1038/nrmicro2381
74. Kolenbrander, P. E. Jr., Palmer, R. J., Rickard, A. H., Jakubovics, N. S., Chalmers, N. I., and Diaz, P. I. (2006). Bacterial interactions and successions during plaque development. Periodontol. 2000 42, 47-79. doi: 10.1111/j.1600-0757.2006.00187.x
75. Koo, H., Xiao, J., Klein, M. I., and Jeon, J. G. (2010). Exopolysaccharides (EPS) produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J. Bacteriol. 192, 3024-3032. doi: 10.1128/JB.01649-09
76. Kreth, J., Merritt, J., Shi, W., and Qi, F. (2005a). Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 187, 7193-203. doi: 10.1128/JB.187.21.7193-7203.2005
77. Kreth, J., Merritt, J., Shi, W., and Qi, F. (2005b). Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol. Microbiol. 57, 392-404. doi: 10.1111/j.1365-2958.2005.04695.x
78. Kuboniwa, M., Hendrickson, E. L., Xia, Q., Wang, T., Xie, H., Hackett, M.,et al. (2009). Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol. 9:98. doi: 10.1186/1471-2180-9-98
79. Kuboniwa, M., and Lamont, R. J. (2010). Subgingival biofilm formation. Periodontol. 2000 52, 38-52. doi: 10.1111/j.1600-0757.2009.00311.x
80. Kuboniwa, M., Tribble, G. D., Lamer, C. E., Killic, A. O., Tao, L., Herzberg, M.,et al. (2006). Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol. Microbiol. 60, 121-139. doi: 10.1111/j.1365-2958.2006.05099.x
81. Kumar, P. S., Griffen, A. L., Moeschberger, M. L., and Leys, E. J. (2005). Identification of candidate periodontal pathogens and beneficial species by quantitative 16S clonal analysis. J. Clin. Microbiol. 43, 3944-3955. doi: 10.1128/JCM.43.8.3944-3955.2005
82. Kuramitsu, H. K., He, X., Lux, R., Anderson, M. H., and Shi, W. (2007). Interspecies interactions within oral microbial communities. Microbiol. Mol. Biol. Rev. 71, 653-670. doi: 10.1128/MMBR.00024-07
83. Kuramitsu, H. K., and Trapa, V. (1984). Genetic exchange between oral streptococci during mixed growth. J. Gen. Microbiol. 130, 2497-2500.
84. Lamont, R. J., EI-Sabaeny, A., Park, Y., Cook, G. S., Costerton, J. W., and Demuth, D. R. (2002). Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gigivalis biofiloms on streptococcal substrates. Microbiology 148, 1627-1636.
85. Lancy, P. Jr., Dirienzo, J. M., Appelbaum, B., Rosan, B., and Holt, S. C. (1983). Corncob formation between Fusobacterium nucleatum and Streptococcus sanguis. Infect. Immun. 40, 303-309.
86. LeBlanc, D. J., Hawley, R. J., Lee, L. N., and Martin, E. J. St. (1978). "Conjugal" transfer of plasmid DNA among oral streptococci. Proc. Natl. Acad. Sci. U.S.A. 75, 3484-3487. doi: 10.1073/pnas.75.7.3484
87. Li, J., Helmerhorst, E. J., Leone, C. W., Troxler, R. F., Yaskell, T., Haffajee, A. D.,et al. (2004). Identification of early microbial colonizers in human dental biofilm. J. Appl. Microbiol. 97, 1311-1318. doi: 10.1111/j.1365-2672.2004.02420.x
88. Li, Y., and Burne, R. A. (2001a). Regulation of the gtfBC and ftf genes of Streptococcus mutans in biofims in response to pH and carbohydrate. Microbiology 147, 2841-2848.
89. Li, Y. H., Lau, P. C. Y., Lee, J. H., Ellen, R. P., and Cvitkovitch, D. G. (2001b). Natural genetic transformation of Streptococcus mutans growing in biofilms. J. Bacteriol. 183, 897-908. doi: 10.1128/JB.183.3.897-908.2001
90. Liu, B., Faller, L. L., Klitgord, N., Mazumdar, V., Ghodsi, M., Sommer, D. D.,et al. (2012). Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS ONE 7:e37919. doi: 10.1371/journal.pone.0037919
91. Loesche, W. J. (1986). Role of Streptococcus mutans in human dental decay. Microbiol. Rev. 50, 353-380.
92. Maeda, K., Nagata, H., Nonaka, A., Kataoka, K., Tanaka, M., and Shizukuishi, S. (2004). Oral streptococcal glyceraldehyde-3-phosphate dehydrogenase mediates interaction with Porphyromonas gingivalis fimbriae. Microbes Infect. 6, 1163-1170. doi: 10.1016/j.micinf.2004.06.005
93. Maeda, K., Tribble, G. D., Tucker, C. M., Anaya, C., Shizukuishi, S., Lewis, J. P.,et al. (2008). A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol. Microbiol. 69, 1153-1164. doi: 10.1111/j.1365-2958.2008.06338.x
94. Marsh, P. D. (1994). Microbial ecology of dental plaque and its significance in health and disease. Adv. Dent. Res. 8, 263-271.
95. Matsumoto-Nakano, M., and Kuramitsu, H. K. (2006). Role of bacteriocin immunity proteins in the antimicrobial sensitivity of Streptococcus mutans. J. Bacteriol. 188, 8095-8102. doi: 10.1128/JB.00908-06
96. McNab, R., Ford, S. K., El-Sabaeny, A., Barbieri, B., Cook, G. S., and Lamont, R. J. (2003). LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185, 274-284. doi: 10.1128/JB.185.1.274-284.2003
97. Merritt, J., Qi, F., Goodman, S. D., Anderson, M. H., and Shi, W. (2003). Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect. Immun. 71, 1972-1979. doi: 10.1128/IAI.71.4.1972-1979.2003
98. Meuric, V., Martin, B., Guyodo, H., Rouillon, A., Tamanai-Shacoori, Z., Barloy-Hubler, F.,et al. (2013). Treponema denticola improves adhesive capacities of Porphyromonas gingivalis. Mol. Oral Microbiol. 28, 40-53. doi: 10.1111/omi.12004
99. Miller, M. B., and Bassler, B. L. (2001). Quorum sensing in bacteria. Annu. Rev. Microbiol. 55, 165-199. doi: 10.1146/annurev.micro.55.1.165
100. Nadell, C. D., Xavier, J. B., and Foster, K. R. (2009). The sociobiology of bio-films. FEMS Microbiol. Rev. 33, 206-224. doi: 10.1111/j.1574-6976.2008.00150.x
101. Nagata, H., Iwasaki, M., Maeda, K., Kuboniwa, M., Hashino, E., Toe, M.,et al. (2009). Identification of the binding domain of Streptococcus oralis glyceraldehyde-3-phosphate dehydrogenase for Porphyromonas gingivalis major fimbriae. Infect. Immun. 77, 5130-5138. doi: 10.1128/IAI.00439-09
102. Nilius, A. M., Spencer, S. C., and Simonson, L. G. (1993). Stimulation of in vitro growth of Treponema denticola by extracellular growth factors produced by Porphyromonas gingivalis. J. Dent. Res. 72, 1027-1031. doi: 10.1177/00220345930720060601
103. Ogawa, A., Furukawa, S., Fujita, S., Mitobe, J., Kawarai, T., Narisawa, N.,et al. (2011). Inhibition of Streptococcus mutans biofilm formation by Streptococcus salivarius FruA. Appl. Environ. Microbiol. 77, 1572-1580. doi: 10.1128/AEM.02066-10
104. Palmer, R. J. Jr., Gordon, S. M., Cisar, J. O., and Kolenbrander, P. E. (2003). Co-aggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J. Bacteriol. 185, 3400-3409. doi: 10.1128/JB.185.11.3400-3409.2003
105. Pangsomboon, K., Bansal, S., Martin, G. P., Suntinanalert, P., Kaewnopparat, S., and Srichana, T. (2009). Further characterization of a bacteriocin produced by Lactobacillus paracasei HL32. J. Appl. Microbiol. 106, 1928-1940. doi: 10.1111/j.1365-2672.2009.04146.x
106. Pangsomboon, K., Kaewnopparat, S., Pitakpornpreecha, T., and Srichana, T. (2006). Antibacterial activity of a bacteriocin from Lactobacillus paracasei HL32 against Porphyromonas gingivalis. Arch. Oral Biol. 51, 784-793. doi: 10.1016/j.archoralbio.2006.03.008
107. Park, Y., James, C. E., Yoshimura, F., and Lamont, R. J. (2006). Expression of the short fimbriae of Porphyromonas gingivalis is regulated in oral bacterial consortia. FEMS Microbiol. Lett. 262, 65-71. doi: 10.1111/j.1574-6968.2006.00357.x
108. Park, Y., Simionato, M. R., Sekiya, K., Murakami, Y., James, D., Chen, W.,et al. (2005). Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect. Immun. 73, 3983-3989. doi: 10.1128/IAI.73.7.3983-3989.2005
109. Paster, B. J., Olsen, I., Aas, J. A., and Dewhirst, F. E. (2006). The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 2, 80-87. doi: 10.1111/j.1600-0757.2006.00174.x
110. Periasamy, S., and Kolenbrander, P. E. (2009a). Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleaum and Veillonella species in saliva. Infect. Immun. 77, 3542-3551. doi: 10.1128/IAI.00345-09
111. Periasamy, S., and Kolenbrander, P. E. (2009b). Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J. Bacteriol. 191, 6804-6811. doi: 10.1128/JB.01006-09
112. Perry, J. A., Cvitkovitch, D. G., and Levesque, C. M. (2009). Cell death in Streptococcus mutans biofilms: a link between CSP and extracellular DNA. FEMS Microbiol. Lett. 299, 261-266. doi: 10.1111/j.1574-6968.2009.01758.x
113. Petersen, F. C., Pecharki, D., and Scheie, A. A. (2004). Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J. Bacteriol. 186, 6327-6331. doi: 10.1128/JB.186.18.6327-6331.2004
114. Qi, F., Chen, P., and Caufield, P. W. (2001). The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl. Environ. Microbiol. 67, 15-21. doi: 10.1128/AEM.67.1.15-21.2001
115. Ramsey, M. M., Rumbaugh, K. P., and Whiteley, M. (2011). Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog. 7:e1002012. doi: 10.1371/journal.ppat.1002012
116. Ramsey, M. M., and Whiteley, M. (2009). Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc. Natl. Acad. Sci. U.S.A. 106, 1578-1583. doi: 10.1073/pnas.0809533106
117. Rice, L. B. (1998). Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob. Agents Chemother. 42, 1871-1877.
118. Rickard, A. H., Palmer, R. J., Blehert, D. S., Campagna, S. R., Semmelhack, M. F., Egland, P. G.,et al. (2006). Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60, 1446-1456. doi: 10.1111/j.1365-2958.2006.05202.x
119. Riedel, K., Hentzer, M., Geisenberger, O., Huber, B., Steidle, A., Wu, H.,et al. (2001). N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147, 3249-3262.
120. Roberts, A. P., and Mullany, P. (2010). Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev. Anti Infect. Ther. 8, 1441-1450. doi: 10.1586/eri.10.106
121. Rölla, G., Scheie, A. A., and Ciardi, J. E. (1985). Role of sucrose in plaque formation. Scand. J. Dent. Res. 93, 105-111.
122. Rosen, G., Genzler, T., and Sela, M. N. (2008). Coaggregation of Treponema denticola with Porphyromonas gingivalis and Fusobacterium nucleatum is mediated by the major outer sheath protein of Treponema denticola. FEMS Microbiol. Lett. 289, 59-66. doi: 10.1111/j.1574-6968.2008.01373.x
123. Rosen, G., and Sela, M. N. (2006). Coaggregation of Porphyromonas gingivalis and Fusobacterium nucleatum PK 1594 is mediated by capsular polysaccharide and lipopolysaccharide. FEMS Microbiol. Lett. 256, 304-310. doi: 10.1111/j.1574-6968.2006.00131.x
124. Rupani, D., Izano, E. A., Schreiner, H. C., Fine, D. H., and Kaplan, J. B. (2008). Aggregatibacter actinomycetemcomitansserotype f O-polysaccharide mediates coaggregation with Fusobacterium nucleatum. Oral Microbiol. Immunol. 23, 127-130. doi: 10.1111/j.1399-302X.2007.00399.x
125. Ryan, R. P., and Dow, J. M. (2008). Diffusible signals and interspecies communication in bacteria. Microbiology 154, 1845-1858. doi: 10.1099/mic.0.2008/017871-0
126. Saito, Y., Fujii, R., Nakagawa, K. I., Kuramitsu, H. K., Okuda, K., and Ishihara, K. (2008). Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol. Immunol. 23, 1-6. doi: 10.1111/j.1399-302X.2007.00380.x
127. Sandmeier, H., van Winkelhoff, A. J., Bär, K., Ankli, E., Maeder, M., and Meyer, J. (1995). Temperate bacteriophages are common among Actinobacillus actinomycetemcomitansisolates from periodontal pockets. J. Periodontol. Res. 30, 418-425. doi: 10.1111/j.1600-0765.1995.tb01296.x
128. Sarkar, J., McHardy, I. H., Simanian, E. J., Shi, W., and Lux, R. (2014). Transcriptional responses of Treponema denticola to other oral bacterial species. PLoS ONE 9:e88361. doi: 10.1371/journal.pone.0088361
129. Schauder, S., and Bassler, B. L. (2001a). The languages of bacteria. Genes Dev. 15, 1468-1480. doi: 10.1101/gad.899601
130. Schauder, S., Shokat, K., Surette, M. G., and Bassler, B. B. (2001b). The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol. Microbiol. 41, 463-476. doi: 10.1046/j.1365-2958.2001.02532.x
131. Schuster, M., Lostroh, C. P., Ogi, T., and Greenberg, E. P. (2003). Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066-2079. doi: 10.1128/JB.185.7.2066-2079.2003
132. Senadheera, D., and Cvitkovitch, D. G. (2008). Quorum sensing and biofilm formation by Streptococcus mutans. Adv. Exp. Med. Biol. 631, 178-188. doi: 10.1007/978-0-387-78885-2_12
133. Senadheera, D., Krastel, K., Mair, R., Persadmehr, A., Abranches, J., Burne, R. A.,et al. (2009). Inactivation of VicK affects acid production and acid survival of Streptococcus mutans. J. Bacteriol. 191, 6415-6424. doi: 10.1128/JB.00793-09
134. Shao, H., Lamont, R. J., and Demuth, D. R. (2007). Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect. Immun. 75, 4211-4218. doi: 10.1128/IAI.00402-07
135. Sharma, A., Inagaki, S., Sigurdson, W., and Kuramitsu, H. K. (2005). Synergy between Tannerella forsythia and Fusobacterium nucleatum in biofilm formation. Oral Microbiol. Immunol. 20, 39-42. doi: 10.1111/j.1399-302X.2004.00175.x
136. Shimotahira, N., Oogai, Y., Kawada-Matsuo, M., Yamada, S., Fukutsuji, K., Nagano, K.,et al. (2013). The surface layer of Tannerella forsythia contributes to serum resistance and oral bacterial coaggregation. Infect. Immun. 81, 1198-1206. doi: 10.1128/IAI.00983-12
137. Simionato, M. R., Tucker, C. M., Kuboniwa, M., Lamont, G., Demuth, D. R., Tribble, G. D.,et al. (2006). Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74, 6419-6428. doi: 10.1128/IAI.00639-06
138. Steeves, C. H., Potrykus, J., Barnett, D. A., and Bearne, S. L. (2011). Oxidative stress response in the opportunistic oral pathogen Fusobacterium nucleatum. Proteomics 11, 2027-2037. doi: 10.1002/pmic.201000631
139. Takahashi, N. (2003). Acid-neutralizing activity during amino acid fermentation by Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol. Immunol. 18, 109-113. doi: 10.1034/j.1399-302X.2003.00054.x
140. Takasaki, K., Fujise, O., Miura, M., Hamachi, T., and Maeda, K. (2013). Porphyromonas gingivalis displays a competitive advantage over Aggregatibacter actinomycetemcomitans in co-cultured biofilm. J. Periodontol. Res. 48, 286-292. doi: 10.1111/jre.12006
141. Takahashi, N., Washio, J., and Mayanagi, G. (2010). Metabolomics of supragingival plaque and oral bacteria. J. Dent. Res. 89, 1383-1388. doi: 10.1177/0022034510377792
142. Tamesada, M., Kawabata, S., Fujiwara, T., and Hamada, S. (2004). Synergistic effects of streptococcal glucosyltransferases on adhesive biofilm formation. J. Dent. Res. 83, 874-879. doi: 10.1177/154405910408301110
143. Tamura, S., Yonezawa, H., Motegi, M., Nakao, R., Yoneda, S., Watanabe, H.,et al. (2009). Inhibiting effects of Streptococcus salivarius on competence-stimulating peptide-dependent biofilm formation by Streptococcus mutans. Oral Microbiol. Immunol. 24, 152-161. doi: 10.1111/j.1399-302X.2008.00489.x
144. Tong, H., Chen, W., Merritt, J., Qi, F., Shi, W., and Dong, X. (2007). Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2: a possible counteroffensive strategy for interspecies competition. Mol. Microbiol. 63, 872-880. doi: 10.1111/j.1365-2958.2006.05546.x
145. Tong, H., Chen, W., Shi, W., Qi, F., and Dong, X. (2008). SO-LAAO, a novel L-amino acid oxidase that enables Streptococcus oligofermentans to outcompete Streptococcus mutans by generating H2O2 from peptone. J. Bacteriol. 190, 4716-4721. doi: 10.1128/JB.00363-08
146. Tong, H., Gao, X., and Dong, X. (2003). Streptococcus oligofermentans sp. nov., a novel oral isolate from caries-free humans. Int. J. Syst. Evol. Microbiol. 53, 1101-1104. doi: 10.1099/ijs.0.02493-0
147. Torres-Escobar, A., Juárez-Rodríguez, M. D., Lamont, R. J., and Demuth, D. R. (2013). Transcriptional regulation of Aggregatibacter actinomycetemcomitans lsrACDBFG and lsrRK operons and their role in biofilm formation. J. Bacteriol. 195, 56-65. doi: 10.1128/JB.01476-12
148. Vacca-Smith, A. M., and Bowen, W. H. (1998). Binding properties of streptococcal glucosyltransferases for hydroxyapatite, saliva-coated hydroxyapatite, and bacterial surfaces. Arch. Oral Biol. 43, 103-110. doi: 10.1016/S0003-9969(97)00111-8
149. van der Hoeven, J. S., and Camp, P. J. (1991). Synergistic degradation of mucin by Streptococcus oralis and Streptococcus sanguis in mixed chemostat cultures. J. Dent. Res. 70, 1041-1044. doi: 10.1177/00220345910700070401
150. Vollaard, E., and Clasener, H. (1994). Colonization resistance. Antimicrob. Agents Chemother. 38, 409-414. doi: 10.1128/AAC.38.3.409
151. Wagner, V. E., Bushnell, D., Passador, L., Brooks, A. I., and Iglewski, B. H. (2003). Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185, 2080-2095. doi: 10.1128/JB.185.7.2080-2095.2003
152. Wang, B. Y., Alvarez, P., Hong, J., and Kuramitsu, H. K. (2011a). Periodontal pathogens interfere with quorum-sensing-dependent virulence properties in Streptococcus mutans. J. Periodontol. Res. 46, 105-110. doi: 10.1111/j.1600-0765.2010.01319.x
153. Wang, B. Y., Deutch, A., Hong, J., and Kuramitsu, H. K. (2011b). Proteases of an early colonizer can hinder Streptococcus mutans colonization in vitro. J. Dent. Res. 90, 501-505. doi: 10.1177/0022034510388808
154. Wang, B. Y., and Kuramitsu, H. K. (2005). Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii. Appl. Environ. Microbiol. 71, 354-362. doi: 10.1128/AEM.71.1.354-362.2005
155. Wang, Q., Wright, C. J., Dingming, H., Uriarte, S. M., Lamont, R. J. (2013). Oral community interactions of Filifactor alocis in vitro. PLoS ONE 8:e76271. doi: 10.1371/journal.pone.0076271
156. Warburton, P. J., Palmer, R. M., Munson, M. A., and Wade, W. G. (2007). Demonstration of in vivo transfer of doxycycline resistance mediated by a novel transposon. J. Antimicrob. Chemother. 60, 973-980. doi: 10.1093/jac/dkm331
157. Whitmore, S. E., and Lamont, R. J. (2011). The pathogenic persona of community-associated oral streptococci. Mol. Microbiol. 81, 305-314. doi: 10.1111/j.1365-2958.2011.07707.x
158. Wickström, C., Herzberg, M. C., Beighton, D., and Svensäter, G. (2009). Proteolytic degradation of human salivary MUC5B by dental biofilms. Microbiology 155, 2866-2872. doi: 10.1099/mic.0.030536-0
159. Xavier, K. B., Bassler, B. L., Xavier, K. B., Miller, S. T., Lu, W., Kim, J. H.,et al. (2007). Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria. ACS Chem. Biol. 2, 128-136. doi: 10.1021/cb600444h
160. Xiao, J., Klein, M. I., Falsetta, M. L., Lu, B., Delahunty, C. M., and Yates, J. R. III,et al. (2012). The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. PLoS Pathog. 8:e1002623. doi: 10.1371/journal.ppat.1002623
161. Xie, H., Lin, X., Wang, B. Y., Wu, J., and Lamont, R. J. (2007). Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153, 3228-3234. doi: 10.1099/mic.0.2007/009050-0
162. Yeung, M. K. (1999). Molecular and genetic analysis of Actinomyces species. Oral Biol. Med. 10, 120-138. doi: 10.1177/10454411990100020101
163. Yim, G., Wang, H. H., and Davies, J. (2006). The truth about antibiotics. Int. J. Med. Microbial. 296, 163-170. doi: 10.1016/j.ijmm.2006.01.039
164. Yuan, L., Hillman, J. D., and Progulske-Fox, A. (2005). Microarray analysis of quorum sensing regulated genes in Porphyromonas gingivalis. Infect. Immun. 73, 4146-4154. doi: 10.1128/IAI.73.7.4146-4154.2005
165. Zainal-Abidin, Z., Veith, P. D., Dashper, S. G., Zhu, Y., Catmull, D. V., Chen, Y. Y.,et al. (2012). Differential proteomic analysis of a polymicrobial biofilm. J. Proteome Res. 11, 4449-4464. doi: 10.1021/pr300201c
166. Zhang, Y., Lei, Y., Khammanivong, A., and Herzberg, M. C. (2004). Identification of a novel two-component system in Streptococcus gordonii V288 involved in biofilm formation. Infect. Immun. 72, 3489-3494. doi: 10.1128/IAI.72.6.3489-3494.2004
167. Zheng, X., Zhang, K., Zhou, X., Liu, C., Li, M., Li, Y.,et al. (2013). Involvement of gshAB in the interspecies competition within oral biofilm. J. Dent. Res. 92, 819-824. doi: 10.1177/0022034513498598
168. Zhu, L., and Kreth, J. (2010). Role of Streptococcus mutans eukaryotic-type serine/threonine protein kinase in interspecies interactions with Streptococcus sanguinis. Arch. Oral Biol. 55, 385-390. doi: 10.1016/j.archoralbio.2010.03.012
169. Zhu, L., and Kreth, J. (2012). The role of hydrogen peroxide in environmental adaptation of oral microbial communities. Oxid. Med. Cell Longev. 2012:717843. doi: 10.1155/2012/717843
170. Zijnge, V., van Leeuwen, M. B., Degener, J. E., Abbas, F., Thurnheer, T., Gmür, R.,et al. (2010). Oral biofilm architecture on natural teeth. PLoS ONE 5:e9321. doi: 10.1371/journal.pone.0009321