Chapter 7 : Fusobacteria as a Bridge between Health and Disease: a Metatranscriptomic Approach

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is an oral anaerobe and the most common gram-negative isolate from both healthy and diseased oral sites. Association of with gingivitis and with its progression to periodontal disease has been based on the fact that numbers of organisms greatly increase in samples taken from diseased sites compared to those from healthy ones. The author feels that the sharing of both gram-positive and gram-negative properties might facilitate communication of fusobacteria with both gram-positive early colonizers and gram-negative late colonizers, an essential stage in the development of the periopathogenic dental biofilm. The species complexity of oral biofilms is probably the greatest hurdle in studying the fusobacterial role in oral health and disease. The author proposes that fusobacterial virulence relies on the presence of its adhesins and not on classical toxins and proteases. Microarrays can be designed to interact uniquely with gene transcripts. These microarrays can be reacted with total RNAs extracted from dental biofilms sampled from healthy and diseased periodontal sites of increasing disease severity. In vitro studies have suggested that fusobacterial bridging coaggregation interactions are important for the shift in the composition of the microbial community associated with transition from health to disease. Ongoing introduction of tools for genetic manipulation of fusobacteria will enable the investigation of fusobacterial virulence-associated molecular elements. Integration species-specific and general molecular tools is expected to enable the study and the understanding of 's role in bridging from oral health to disease.

Citation: Bachrach G, Coppenhagen-Glazer S, Simon I. 2011. Fusobacteria as a Bridge between Health and Disease: a Metatranscriptomic Approach, p 93-102. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch7
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Linear preferential amplification and reverse transcription of total community mRNA. Redrawn from http://www.ambion.com with permission. aRNA, antisense RNA.

Citation: Bachrach G, Coppenhagen-Glazer S, Simon I. 2011. Fusobacteria as a Bridge between Health and Disease: a Metatranscriptomic Approach, p 93-102. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch7
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1. Bachrach, G.,, S. K. Haake,, A. Glick,, R. Hazan,, R. Naor,, R. N. Andersen, and, P. E. Kolenbrander. 2004. Characterization of the novel Fusobacterium nucleatum plasmid pKH9 and evidence of an addiction system. Appl. Environ. Microbiol. 70: 69576962.
2. Bachrach, G.,, C. Ianculovici,, R. Naor, and, E. I. Weiss. 2005. Fluorescence based measurements of Fusobacterium nucleatum coaggregation and of fusobacterial attachment to mammalian cells. FEMS Microbiol. Lett. 248: 235240.
3. Bachrach, G.,, G. Rosen,, M. Bellalou,, R. Naor, and, M. N. Sela. 2004. Identification of a Fusobacterium nucleatum 65 kDa serine protease. Oral Microbiol. Immunol. 19: 155159.
4. Baker, P. J.,, R. T. Evans, and, D. C. Roopenian. 1994. Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch. Oral Biol. 39: 10351040.
5. Darenfed, H.,, D. Grenier, and, D. Mayrand. 1999. Acquisition of plasmin activity by Fusobacterium nucleatum subsp. nucleatum and potential contribution to tissue destruction during periodontitis. Infect. Immun. 67: 64396444.
6. Demuth, D. R.,, R. Savary,, E. Golub, and, B. J. Shenker. 1996. Identification and analysis of fipA, a Fusobacterium nucleatum immunosuppressive factor gene. Infect. Immun. 64: 13351341.
7. Drepper, T.,, T. Eggert,, F. Circolone,, A. Heck,, U. Krauss,, J. K. Guterl,, M. Wendorff,, A. Losi,, W. Gartner, and, K. E. Jaeger. 2007. Reporter proteins for in vivo fluorescence without oxygen. Nat. Biotechnol. 25: 443445.
8. Egland, P. G.,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2004. Interspecies communication in Streptococcus gordonii- Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. USA 101: 1691716922.
9. Eid, J.,, A. Fehr,, J. Gray,, K. Luong,, J. Lyle,, G. Otto,, P. Peluso,, D. Rank,, P. Baybayan,, B. Bettman,, A. Bibillo,, K. Bjornson,, B. Chaudhuri,, F. Christians,, R. Cicero,, S. Clark,, R. Dalal,, A. Dewinter,, J. Dixon,, M. Foquet,, A. Gaertner,, P. Hardenbol,, C. Heiner,, K. Hester,, D. Holden,, G. Kearns,, X. Kong,, R. Kuse,, Y. Lacroix,, S. Lin,, P. Lundquist,, C. Ma,, P. Marks,, M. Maxham,, D. Murphy,, I. Park,, T. Pham,, M. Phillips,, J. Roy,, R. Sebra,, G. Shen,, J. Sorenson,, A. Tomaney,, K. Travers,, M. Trulson,, J. Vieceli,, J. Wegener,, D. Wu,, A. Yang,, D. Zaccarin,, P. Zhao,, F. Zhong,, J. Korlach, and, S. Turner. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323: 133138.
10. Frias, J.,, E. Olle, and, M. Alsina. 2001. Periodontal pathogens produce quorum sensing signal molecules. Infect. Immun. 69: 34313434.
11. Frias-Lopez, J.,, Y. Shi,, G. W. Tyson,, M. L. Coleman,, S. C. Schuster,, S. W. Chisholm, and, E. F. Delong. 2008. Microbial community gene expression in ocean surface waters. Proc. Natl. Acad. Sci. USA 105: 38053810.
12. Graves, D. T.,, D. Fine,, Y. T. Teng,, T. E. Van Dyke, and, G. Hajishengallis. 2008. The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J. Clin. Periodontol. 35: 89105.
13. Grenier, D.,, and L. Grignon. 2006. Response of human macrophage-like cells to stimulation by Fusobacterium nucleatum ssp. nucleatum lipopolysaccharide. Oral Microbiol. Immunol. 21: 190196.
14. Guo, M.,, Y. W. Han,, A. Sharma, and, E. De Nardin. 2000. Identification and characterization of human immunoglobulin G Fc receptors of Fusobacterium nucleatum. Oral Microbiol. Immunol. 15: 119123.
15. Haake, S. K.,, S. C. Yoder,, G. Attarian, and, K. Podkaminer. 2000. Native plasmids of Fusobacterium nucleatum: characterization and use in development of genetic systems. J. Bacteriol. 182: 11761180.
16. Han, Y. W.,, A. Ikegami,, P. Chung,, L. Zhang, and, C. X. Deng. 2007. Sonoporation is an efficient tool for intracellular fluorescent dextran delivery and one-step double-crossover mutant construction in Fusobacterium nucleatum. Appl. Environ. Microbiol. 73: 36773683.
17. Han, Y. W.,, A. Ikegami,, C. Rajanna,, H. I. Kawsar,, Y. Zhou,, M. Li,, H. T. Sojar,, R. J. Genco,, H. K. Kuramitsu, and, C. X. Deng. 2005. Identification and characterization of a novel adhesin unique to oral fusobacteria. J. Bacteriol. 187: 53305340.
18. Han, Y. W.,, W. Shi,, G. T. Huang,, S. Kinder Haake,, N. H. Park,, H. Kuramitsu, and, R. J. Genco. 2000. Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect. Immun. 68: 31403146.
19. Hashimoto, S.,, W. Qu,, B. Ahsan,, K. Ogoshi,, A. Sasaki,, Y. Nakatani,, Y. Lee,, M. Ogawa,, A. Ametani,, Y. Suzuki,, S. Sugano,, C. C. Lee,, R. C. Nutter,, S. Morishita, and, K. Matsushima. 2009. High-resolution analysis of the 5′-end transcriptome using a next generation DNA sequencer. PLoS ONE 4: e4108.
20. Hill, G. B. 1993. Investigating the source of amniotic fluid isolates of fusobacteria. Clin. Infect. Dis. 16 (Suppl. 4): S423S424.
21. Hill, G. B. 1998. Preterm birth: associations with genital and possibly oral microflora. Ann. Periodontol. 3: 222232.
22. Kapatral, V.,, I. Anderson,, N. Ivanova,, G. Reznik,, T. Los,, A. Lykidis,, A. Bhattacharyya,, A. Bartman,, W. Gardner,, G. Grechkin,, L. Zhu,, O. Vasieva,, L. Chu,, Y. Kogan,, O. Chaga,, E. Goltsman,, A. Bernal,, N. Larsen,, M. D’Souza,, T. Walunas,, G. Pusch,, R. Haselkorn,, M. Fonstein,, N. Kyrpides, and, R. Overbeek. 2002. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 184: 20052018.
23. Kapatral, V.,, N. Ivanova,, I. Anderson,, G. Reznik,, A. Bhattacharyya,, W. L. Gardner,, N. Mikhailova,, A. Lapidus,, N. Larsen,, M. D’Souza,, T. Walunas,, R. Haselkorn,, R. Overbeek, and, N. Kyrpides. 2003. Genome analysis of F. nucleatum sub spp vincentii and its comparison with the genome of F. nucleatum ATCC 25586. Genome Res. 13: 11801189.
24. Kaplan, C. W.,, R. Lux,, S. K. Haake, and, W. Shi. 2009. The Fusobacterium nucleatum outer membrane protein RadD is an arginineinhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol. 71: 3547.
25. Kaplan, C. W.,, R. Lux,, T. Huynh,, A. Jewett,, W. Shi, and, S. K. Haake. 2005. Fusobacterium nucleatum apoptosis-inducing outer membrane protein. J. Dent. Res. 84: 700704.
26. Karpathy, S. E.,, X. Qin,, J. Gioia,, H. Jiang,, Y. Liu,, J. F. Petrosino,, S. Yerrapragada,, G. E. Fox,, S. K. Haake,, G. M. Weinstock, and, S. K. Highlander. 2007. Genome sequence of Fusobacterium nucleatum subspecies polymorphum—a genetically tractable fusobacterium. PLoS ONE 2: e659.
27. Kolenbrander, P. E.,, and R. N. Andersen. 1989. Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas ( Bacteroides) gingivalis by lactose and related sugars. Infect. Immun. 57: 32043209.
28. 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.
29. Kolenbrander, P. E.,, N. S. Jakubovics,, N. I. Chalmers, and, G. Bachrach. 2007. Coaggregation and distance-critical communication, p. 89–100. In K. A. Brogden,, F. C. Minion,, N. Cornick,, T. B. Stanton,, K. Zhang,, L. K. Nolan, and, M. J. Wannemuehler (ed.), Virulence Mechanisms of Bacterial Pathogens, 4th ed. ASM Press, Washington, DC.
30. Kolenbrander, P. E.,, K. D. Parrish,, R. N. Andersen, and, E. P. Greenberg. 1995. Intergeneric coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp. Infect. Immun. 63: 45844588.
31. Liu, H.,, R. W. Redline, and, Y. W. Han. 2007. Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J. Immunol. 179: 25012508.
32. Mao, C.,, C. Evans,, R. V. Jensen, and, B. W. Sobral. 2008. Identification of new genes in Sinorhizobium meliloti using the Genome Sequencer FLX system. BMC Microbiol. 8: 72.
33. Mardis, E. R. 2008. Next-generation DNA sequencing methods. Annu. Rev. Genomics Hum. Genet. 9: 387402.
34. Margulies, M.,, M. Egholm,, W. E. Altman,, S. Attiya,, J. S. Bader,, L. A. Bemben,, J. Berka,, M. S. Braverman,, Y. J. Chen,, Z. Chen,, S. B. Dewell,, L. Du,, J. M. Fierro,, X. V. Gomes,, B. C. Godwin,, W. He,, S. Helgesen,, C. H. Ho,, G. P. Irzyk,, S. C. Jando,, M. L. Alenquer,, T. P. Jarvie,, K. B. Jirage,, J. B. Kim,, J. R. Knight,, J. R. Lanza,, J. H. Leamon,, S. M. Lefkowitz,, M. Lei,, J. Li,, K. L. Lohman,, H. Lu,, V. B. Makhijani,, K. E. McDade,, M. P. McKenna,, E. W. Myers,, E. Nickerson,, J. R. Nobile,, R. Plant,, B. P. Puc,, M. T. Ronan,, G. T. Roth,, G. J. Sarkis,, J. F. Simons,, J. W. Simpson,, M. Srinivasan,, K. R. Tartaro,, A. Tomasz,, K. A. Vogt,, G. A. Volkmer,, S. H. Wang,, Y. Wang,, M. P. Weiner,, P. Yu,, R. F. Begley, and, J. M. Rothberg. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376380.
35. Mira, A.,, R. Pushker,, B. A. Legault,, D. Moreira, and, F. Rodriguez-Valera. 2004. Evolutionary relationships of Fusobacterium nucleatum based on phylogenetic analysis and comparative genomics. BMC Evol. Biol. 4: 50.
36. Moore, W. E.,, and L. V. Moore. 1994. The bacteria of periodontal diseases. Periodontol. 2000 5: 6677.
37. Morozova, O.,, and M. A. Marra. 2008. Applications of next-generation sequencing technologies in functional genomics. Genomics 92: 255264.
38. Nithianantham, S.,, M. Xu,, M. Yamada,, A. Ikegami,, M. Shoham, and, Y. W. Han. 2009. Crystal structure of FadA adhesin from Fusobacterium nucleatum reveals a novel oligomerization motif, the leucine chain. J. Biol. Chem. 284: 38653872.
39. Nyvad, B.,, and M. Kilian. 1987. Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand. J. Dent. Res. 95: 369380.
40. Palmer, R. J.,, Jr., K. Kazmerzak,, M. C. Hansen, and, P. E. Kolenbrander. 2001. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect. Immun. 69: 57945804.
41. Park, Y.,, C. E. James,, F. Yoshimura, and, R. J. Lamont. 2006. Expression of the short fimbriae of Porphyromonas gingivalis is regulated in oral bacterial consortia. FEMS Microbiol. Lett. 262: 6571.
42. Paster, B. J.,, S. K. Boches,, J. L. Galvin,, R. E. Ericson,, C. N. Lau,, V. A. Levanos,, A. Sahasrabudhe, and, F. E. Dewhirst. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183: 37703783.
43. Rickard, A. H.,, R. J. Palmer, Jr.,, D. S. Blehert,, S. R. Campagna,, M. F. Semmelhack,, P. G. Egland,, B. L. Bassler, and, P. E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60: 14461456.
44. Rogers, A. H.,, P. S. Zilm,, N. J. Gully,, A. L. Pfennig, and, P. D. Marsh. 1991. Aspects of the growth and metabolism of Fusobacterium nucleatum ATCC 10953 in continuous culture. Oral Microbiol. Immunol. 6: 250255.
45. Socransky, S. S.,, A. D. Haffajee,, M. A. Cugini,, C. Smith, and, R. L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25: 134144.
46. Torres, T. T.,, M. Metta,, B. Ottenwalder, and, C. Schlotterer. 2008. Gene expression profiling by massively parallel sequencing. Genome Res. 18: 172177.
47. Uitto, V. J.,, D. Baillie,, Q. Wu,, R. Gendron,, D. Grenier,, E. E. Putnins,, A. Kanervo, and, J. D. Firth. 2005. Fusobacterium nucleatum increases collagenase 3 production and migration of epithelial cells. Infect. Immun. 73: 11711179.
48. Weiss, E. I.,, B. Shaniztki,, M. Dotan,, N. Ganeshkumar,, P. E. Kolenbrander, and, Z. Metzger. 2000. Attachment of Fusobacterium nucleatum PK1594 to mammalian cells and its coaggregation with periodontopathogenic bacteria are mediated by the same galactose-binding adhesin. Oral Microbiol. Immunol. 15: 371377.
49. Wilensky, A.,, Y. Gabet,, H. Yumoto,, Y. Houri-Haddad, and, L. Shapira. 2005. Threedimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J. Periodontol. 76: 12821286.

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