Skip to main content
SpringerLink
Log in

Characterization of aid1, a Novel Gene Involved in Fusobacterium nucleatum Interspecies Interactions

  • Genes and Genomes
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The oral opportunistic pathogen Fusobacterium nucleatum is known to interact with a large number of different bacterial species residing in the oral cavity. It adheres to a variety of Gram-positive bacteria, including oral streptococci via the arginine-inhibitable adhesin RadD. In this study, we describe a novel protein encoded by the predicted open reading frame FN1253 that appears to play a role in interspecies interactions of F. nucleatum, particularly with oral streptococci and related Gram-positive species. We designated FN1253 as aid1 (Adherence Inducing Determinant 1). Expression analyses demonstrated that this gene was induced in F. nucleatum single species biofilms, while the presence of representative members of the oral microbiota known to adhere to F. nucleatum triggered its suppression. Inactivation as well as overexpression of aid1 affected the ability of F. nucleatum to coaggregate with oral streptococci and the closely related Enterococcus faecalis, but not other Gram-positive oral species tested. Furthermore, overexpression of aid1 led to a drastic change in the structure of dual species biofilms of F. nucleatum with oral streptococci. Aid1 function was abolished in the presence of arginine and found to be dependent on RadD. Interestingly, differential expression of aid1 did not affect messenger RNA and protein levels of RadD. These findings indicate that RadD-mediated adhesion to oral streptococci involves more complex cellular processes than the simple interaction of adhesins on the surface of partner strains. Aid1 could potentially play an important role in facilitating RadD-mediated interaction with oral streptococci by increasing binding specificity of F. nucleatum to other microbial species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG (2010) The human oral microbiome. J Bacteriol 192(19):5002–5017. doi:10.1128/JB.00542-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43(11):5721–5732. doi:10.1128/JCM.43.11.5721-5732.2005

    Article  PubMed Central  PubMed  Google Scholar 

  3. Kolenbrander PE, London J (1993) Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175(11):3247–3252

    PubMed Central  CAS  PubMed  Google Scholar 

  4. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ (2002) Communication among oral bacteria. Microbiol Mol Biol Rev 66(3):486–505. doi:10.1128/mmbr.66.3.486-505.2002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Bastos JA, Diniz CG, Bastos MG, Vilela EM, Silva VL, Chaoubah A, Souza-Costa DC, Andrade LC (2011) Identification of periodontal pathogens and severity of periodontitis in patients with and without chronic kidney disease. Arch Oral Biol 56(8):804–811. doi:10.1016/j.archoralbio.2010.12.006

    Article  PubMed  Google Scholar 

  6. Gonzalez OA, Li M, Ebersole JL, Huang CB (2010) HIV-1 reactivation induced by the periodontal pathogens Fusobacterium nucleatum and Porphyromonas gingivalis involves toll-like receptor 2 [corrected] and 9 activation in monocytes/macrophages. CVI 17(9):1417–1427. doi:10.1128/CVI.00009-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  7. Hsiao WW, Li KL, Liu Z, Jones C, Fraser-Liggett CM, Fouad AF (2012) Microbial transformation from normal oral microbiota to acute endodontic infections. BMC Genomics 13:345. doi:10.1186/1471-2164-13-345

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Lee HR, Jun HK, Kim HD, Lee SH, Choi BK (2012) Fusobacterium nucleatum GroEL induces risk factors of atherosclerosis in human microvascular endothelial cells and ApoE(−/−) mice. Mol Oral Microbiol 27(2):109–123. doi:10.1111/j.2041-1014.2011.00636.x

    Article  CAS  PubMed  Google Scholar 

  9. Okada M, Awane S, Suzuki J, Hino T, Takemoto T, Kurihara H, Miura K (2002) Microbiological, immunological and genetic factors in family members with periodontitis as a manifestation of systemic disease, associated with hematological disorders. J Periodontal Res 37(4):307–315

    Article  PubMed  Google Scholar 

  10. Sparks Stein P, Steffen MJ, Smith C, Jicha G, Ebersole JL, Abner E, Dawson D 3rd (2012) Serum antibodies to periodontal pathogens are a risk factor for Alzheimer’s disease. Alzheimers Dement JAlzheimer Assoc 8(3):196–203. doi:10.1016/j.jalz.2011.04.006

    Article  CAS  Google Scholar 

  11. Han YW, Wang X (2013) Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J Dent Res 92(6):485–491

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Kaplan CW, Lux R, Haake SK, 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(1):35–47. doi:10.1111/j.1365-2958.2008.06503.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. McHardy IH (2011) Analysis of interspecies interactions of periodontal bacteria using microarrays. Ph D, UCLA

  14. Kapatral V, Anderson I, Ivanova N, Reznik G, Los T, Lykidis A, Bhattacharyya A, Bartman A, Gardner W, Grechkin G, Zhu L, Vasieva O, Chu L, Kogan Y, Chaga O, Goltsman E, Bernal A, Larsen N, D'Souza M, Walunas T, Pusch G, Haselkorn R, Fonstein M, Kyrpides N, Overbeek R (2002) Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184(7):2005–2018

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Ohta K, Makinen KK, Loesche WJ (1986) Purification and characterization of an enzyme produced by Treponema denticola capable of hydrolyzing synthetic trypsin substrates. Infect Immun 53(1):213–220

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Kaplan CW, Lux R, Huynh T, Jewett A, Shi W, Haake SK (2005) Fusobacterium nucleatum apoptosis-inducing outer membrane protein. J Dent Res 84(8):700–704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Haake SK, Yoder SC, Attarian G, Podkaminer K (2000) Native plasmids of Fusobacterium nucleatum: characterization and use in development of genetic systems. J Bacteriol 182(4):1176–1180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Cisar JO, Kolenbrander PE, McIntire FC (1979) Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun 24(3):742–752

    PubMed Central  CAS  PubMed  Google Scholar 

  19. Kolenbrander PE, Andersen RN, Moore LV (1990) Intrageneric coaggregation among strains of human oral bacteria: potential role in primary colonization of the tooth surface. Appl Environ Microbiol 56(12):3890–3894

    PubMed Central  CAS  PubMed  Google Scholar 

  20. Kolenbrander PE, Andersen RN (1989) Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect Immun 57(10):3204–3209

    PubMed Central  CAS  PubMed  Google Scholar 

  21. Whittaker CJ, Klier CM, Kolenbrander PE (1996) Mechanisms of adhesion by oral bacteria. Annu Rev Microbiol 50:513–552. doi:10.1146/annurev.micro.50.1.513

    Article  CAS  PubMed  Google Scholar 

  22. Takemoto T, Hino T, Yoshida M, Nakanishi K, Shirakawa M, Okamoto H (1995) Characteristics of multimodal co-aggregation between Fusobacterium nucleatum and streptococci. J Periodontal Res 30(4):252–257

    Article  CAS  PubMed  Google Scholar 

  23. ten Cate JM (2006) Biofilms, a new approach to the microbiology of dental plaque. Odontology 94(1):1–9. doi:10.1007/s10266-006-0063-3

    Article  PubMed  Google Scholar 

  24. Kolenbrander PE (1993) Coaggregation of human oral bacteria: potential role in the accretion of dental plaque. J Appl Bacteriol 74(Suppl):79S–86S

    Article  PubMed  Google Scholar 

  25. Zijnge V, van Leeuwen MB, Degener JE, Abbas F, Thurnheer T, Gmur R, Harmsen HJ (2010) Oral biofilm architecture on natural teeth. PLoS ONE 5(2):e9321. doi:10.1371/journal.pone.0009321

    Article  PubMed Central  PubMed  Google Scholar 

  26. Kim S, Jeon TJ, Oberai A, Yang D, Schmidt JJ, Bowie JU (2005) Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc Natl Acad Sci U S A 102(40):14278–14283. doi:10.1073/pnas.0501234102

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Barwe SP, Kim S, Rajasekaran SA, Bowie JU, Rajasekaran AK (2007) Janus model of the Na, K-ATPase beta-subunit transmembrane domain: distinct faces mediate alpha/beta assembly and beta-beta homo-oligomerization. J Mol Biol 365(3):706–714. doi:10.1016/j.jmb.2006.10.029

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  28. Plotkowski ML, Kim S, Phillips ML, Partridge AW, Deber CM, Bowie JU (2007) Transmembrane domain of myelin protein zero can form dimers: possible implications for myelin construction. Biochemistry 46(43):12164–12173. doi:10.1021/bi701066h

    Article  CAS  PubMed  Google Scholar 

  29. Han YW, Ikegami A, Rajanna C, Kawsar HI, Zhou Y, Li M, Sojar HT, Genco RJ, Kuramitsu HK, Deng CX (2005) Identification and characterization of a novel adhesin unique to oral fusobacteria. J Bacteriol 187(15):5330–5340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Xu M, Yamada M, Li M, Liu H, Chen SG, Han YW (2007) FadA from Fusobacterium nucleatum utilizes both secreted and nonsecreted forms for functional oligomerization for attachment and invasion of host cells. J Biol Chem 282(34):25000–25009

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The pHS58 shuttle plasmid was kindly provided by Dr. Susan Kinder Haake. This work is supported by the Whitcome Pre-doctoral Training Grant to AK and NIH/NIDCR grant DE021108 to RL.

Author information

Authors and Affiliations

  1. UCLA Department of Microbiology, Immunology and Molecular Genetics, Los Angeles, CA, 90095, USA

    Aida Kaplan & Wenyuan Shi

  2. C3-Jian, Inc, Marina del Rey, CA, 90292, USA

    Christopher W. Kaplan & Wenyuan Shi

  3. UCLA School of Dentistry, 10833 Le Conte Avenue, CHS 33-080, Los Angeles, CA, 90095-1668, USA

    Xuesong He, Wenyuan Shi & Renate Lux

  4. UCLA David Geffen School of Medicine, Los Angeles, CA, 90095, USA

    Ian McHardy

Authors
  1. Aida Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher W. Kaplan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuesong He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ian McHardy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenyuan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Renate Lux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renate Lux.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Fig. 1

Construction of aid1 mutant strains. A. Construction of Δaid1 inactivation strain. aid1 was inactivated via double homologous recombination by inserting a catP thiamphenicol/chloramphenicol resistance cassette into the aid1 gene. B. Construction of Fn/pEP-aid1 and radD/pEP-aid1 overexpression strains. aid1 was overexpressed in wild type F. nucleatum ATCC 23726 and in radD strains by introducing a shuttle plasmid carrying aid1 gene with its own endogenous promoter into wild type F. nucleatum ATCC 23726 and ΔradD strains respectively. (PPTX 52 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaplan, A., Kaplan, C.W., He, X. et al. Characterization of aid1, a Novel Gene Involved in Fusobacterium nucleatum Interspecies Interactions. Microb Ecol 68, 379–387 (2014). https://doi.org/10.1007/s00248-014-0400-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-014-0400-y

Keywords

Search

Navigation