Log in

Short-chain fatty acids inhibit the biofilm formation of Streptococcus gordonii through negative regulation of competence-stimulating peptide signaling pathway

  • Microbial Pathogenesis and Host-Microbe Interaction
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Streptococcus gordonii, a Gram-positive commensal bacterium, is an opportunistic pathogen closely related to initiation and progression of various oral diseases, such as periodontitis and dental caries. Its biofilm formation is linked with the development of such diseases by enhanced resistance against antimicrobial treatment or host immunity. In the present study, we investigated the effect of short-chain fatty acids (SCFAs) on the biofilm formation of S. gordonii. SCFAs, including sodium acetate (NaA), sodium propionate (NaP), and sodium butyrate (NaB), showed an effective inhibitory activity on the biofilm formation of S. gordonii without reduction in bacterial growth. SCFAs suppressed S. gordonii biofilm formation at early time points whereas SCFAs did not affect its preformed biofilm. A quorum-sensing system mediated by competence-stimulating peptide (CSP) is known to regulate biofilm formation of streptococci. Interestingly, SCFAs substantially decreased mRNA expression of comD and comE, which are CSP-sensor and its response regulator responsible for CSP pathway, respectively. Although S. gordonii biofilm formation was enhanced by exogenous synthetic CSP treatment, such effect was not observed in the presence of SCFAs. Collectively, these results suggest that SCFAs have an anti-biofilm activity on S. gordonii through inhibiting comD and comE expression which results in negative regulation of CSP quorum-sensing system. SCFAs could be an effective anti-biofilm agent against S. gordonii for the prevention of oral diseases.

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

Access this article

Price includes VAT (Canada)

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abranches, J., Zeng, L., Kajfasz, J.K., Palmer, S.R., Chakraborty, B., Wen, Z.T., Richards, V.P., Brady, L.J., and Lemos, J.A. 2018. Biology of oral streptococci. Microbiol. Spectr. 6. doi:https://doi.org/10.1128/microbiolspec.GPP3-0042-2018.

  • Aggarwal, S.D., Yesilkaya, H., Dawid, S., and Hiller, N.L. 2020. The pneumococcal social network. PLoS Pathog. 16, e1008931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amrutha, B., Sundar, K., and Shetty, P.H. 2017. Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb. Pathog. 111, 156–162.

    Article  CAS  PubMed  Google Scholar 

  • Back, C.R., Sztukowska, M.N., Till, M., Lamont, R.J., Jenkinson, H.F., Nobbs, A.H., and Race, P.R. 2017. The Streptococcus gordonii adhesin cshA protein binds host fibronectin via a catch-clamp mechanism. J. Biol. Chem. 292, 1538–1549.

    Article  CAS  PubMed  Google Scholar 

  • Bramante, C.M., Luna-Cruz, S.M., Sipert, C.R., Bernadineli, N., Garcia, R.B., de Moraes, I.G., and de Vasconcelos, B.C. 2008. Alveolar mucosa necrosis induced by utilisation of calcium hydroxide as root canal dressing. Int. Dent. J. 58, 81–85.

    Article  PubMed  Google Scholar 

  • Chen, Y., Gozzi, K., Yan, F., and Chai, Y. 2015. Acetic acid acts as a volatile signal to stimulate bacterial biofilm formation. mBio 6, e00392–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, J., Hu, H., Fang, W., Shi, D., Liang, C., Sun, Y., Gao, G., Wang, H., Zhang, Q., Wang, L., et al. 2019. Detection of pathogens from resected heart valves of patients with infective endocarditis by next-generation sequencing. Int. J. Infect. Dis. 83, 148–153.

    Article  CAS  PubMed  Google Scholar 

  • Cummings, J.H., Pomare, E.W., Branch, W.J., Naylor, C.P., and Macfarlane, G.T. 1987. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 28, 1221–1227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davey, L., Halperin, S.A., and Lee, S.F. 2016. Mutation of the Streptococcus gordonii thiol-disulfide oxidoreductase sdbA leads to enhanced biofilm formation mediated by the ciaRH two-component signaling system. PLoS ONE 11, e0166656.

    Article  PubMed  PubMed Central  Google Scholar 

  • Domenech, M., Ramos-Sevillano, E., García, E., Moscoso, M., and Yuste, J. 2013. Biofilm formation avoids complement immunity and phagocytosis of Streptococcus pneumoniae. Infect. Immun. 81, 2606–2615.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, Y., Chen, Y.Y., Snyder, J.A., and Burne, R.A. 2002. Isolation and molecular analysis of the gene cluster for the arginine deiminase system from Streptococcus gordonii DL1. Appl. Environ. Microbiol. 68, 5549–5553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flemming, H.C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S.A., and Kjelleberg, S. 2016. Biofilms: an emergent form of bacterial life. Nat. Rev. Microbiol. 14, 563–575.

    Article  CAS  PubMed  Google Scholar 

  • Gürgan, C.A., Zaim, E., Bakirsoy, I., and Soykan, E. 2006. Short-term side effects of 0.2% alcohol-free chlorhexidine mouthrinse used as an adjunct to non-surgical periodontal treatment: a double-blind clinical study. J. Periodontol. 77, 370–384.

    Article  PubMed  Google Scholar 

  • Halstead, F.D., Rauf, M., Moiemen, N.S., Bamford, A., Wearn, C.M., Fraise, A.P., Lund, P.A., Oppenheim, B.A., and Webber, M.A. 2015. The antibacterial activity of acetic acid against biofilm-producing pathogens of relevance to burns patients. PLoS ONE 10, e0136190.

    Article  PubMed  PubMed Central  Google Scholar 

  • Heng, N.C.K., Tagg, J.R., and Tompkins, G.R. 2006. Identification and characterization of the loci encoding the competence-associated alternative sigma factor of Streptococcus gordonii. FEMS Microbiol. Lett. 259, 27–34.

    Article  CAS  PubMed  Google Scholar 

  • Jack, A.A., Daniels, D.E., Jepson, M.A., Vickerman, M.M., Lamont, R.J., Jenkinson, H.F., and Nobbs, A.H. 2015. Streptococcus gordonii comCDE (competence) operon modulates biofilm formation with Candida albicans. Microbiology 161, 411–421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jani, S., Seely, A.L., Peabody V, G.L., Jayaraman, A., and Manson, M.D. 2017. Chemotaxis to self-generated AI-2 promotes biofilm formation in Escherichia coli. Microbiology 163, 1778–1790.

    Article  CAS  PubMed  Google Scholar 

  • Jolkver, E., Emer, D., Ballan, S., Krämer, R., Eikmanns, B.J., and Marin, K. 2009. Identification and characterization of a bacterial transport system for the uptake of pyruvate, propionate, and acetate in Corynebacterium glutamicum. J. Bacteriol. 191, 940–948.

    Article  CAS  PubMed  Google Scholar 

  • Kim, A.R., Ahn, K.B., Yun, C.H., Park, O.J., Perinpanayagam, H., Yoo, Y.J., Kum, K.Y., and Han, S.H. 2019. Lactobacillus plantarum lipoteichoic acid inhibits oral multispecies biofilm. J. Endod. 45, 310–315.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Kostakioti, M., Hadjifrangiskou, M., and Hultgren, S.J. 2013. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect. Med. 3, a010306.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouidhi, B., Al Qurashi, Y.M., and Chaieb, K. 2015. Drug resistance of bacterial dental biofilm and the potential use of natural compounds as alternative for prevention and treatment. Microb. Pathog. 80, 39–49.

    Article  CAS  PubMed  Google Scholar 

  • Kundukad, B., Schussman, M., Yang, K., Seviour, T., Yang, L., Rice, S.A., Kjelleberg, S., and Doyle, P.S. 2017. Mechanistic action of weak acid drugs on biofilms. Sci. Rep. 7, 4783.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamas, A., Regal, P., Vázquez, B., Cepeda, A., and Franco, C.M. 2019. Short chain fatty acids commonly produced by gut microbiota influence Salmonella enterica motility, biofilm formation, and gene expression. Antibiotics 8, 265.

    Article  CAS  PubMed Central  Google Scholar 

  • Lemme, A., Gröbe, L., Reck, M., Tomasch, J., and Wagner-Döbler, I. 2011. Subpopulation-specific transcriptome analysis of competence-stimulating-peptide-induced Streptococcus mutans. J. Bacteriol. 193, 1863–1877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, C., Sun, D., Zhu, J., Liu, J., and Liu, W. 2020. The regulation of bacterial biofilm formation by cAMP-CRP: a mini-review. Front. Microbiol. 11, 802.

    Article  PubMed  PubMed Central  Google Scholar 

  • Loo, C.Y., Corliss, D.A., and Ganeshkumar, N. 2000. Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. J. Bacteriol. 182, 1374–1382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu, R., Meng, H., Gao, X., Xu, L., and Feng, X. 2014. Effect of non-surgical periodontal treatment on short chain fatty acid levels in gingival crevicular fluid of patients with generalized aggressive periodontitis. J. Periodontal. Res. 49, 574–583.

    Article  CAS  PubMed  Google Scholar 

  • Macfarlane, S. and Macfarlane, G.T. 2003. Regulation of short-chain fatty acid production. Proc. Nutr. Soc. 62, 67–72.

    Article  CAS  PubMed  Google Scholar 

  • Marquis, R.E., Bender, G.R., Murray, D.R., and Wong, A. 1987. Arginine deiminase system and bacterial adaptation to acid environments. Appl. Environ. Microbiol. 53, 198–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsh, P.D. and Bradshaw, D.J. 1995. Dental plaque as a biofilm. J. Ind. Microbiol. 15, 169–175.

    Article  CAS  PubMed  Google Scholar 

  • Muhammad, M.H., Idris, A.L., Fan, X., Guo, Y., Yu, Y., **, X., Qiu, J., Guan, X., and Huang, T. 2020. Beyond risk: bacterial biofilms and their regulating approaches. Front. Microbiol. 11, 928.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagasawa, R., Yamamoto, T., Utada, A.S., Nomura, N., and Obana, N. 2020. Competence-stimulating-peptide-dependent localized cell death and extracellular DNA production in Streptococcus mutans biofilms. Appl. Environ. Microbiol. 86, e02080–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura, K., O’Neill, A.M., Williams, M.R., Cau, L., Nakatsuji, T., Horswill, A.R., and Gallo, R.L. 2020. Short chain fatty acids produced by Cutibacterium acnes inhibit biofilm formation by Staphylococcus epidermidis. Sci. Rep. 10, 21237.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nobbs, A.H., Lamont, R.J., and Jenkinson, H.F. 2009. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73, 407–450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, O.J., Jung, S., Park, T., Kim, A.R., Lee, D., Ji, H.J., Seo, H.S., Yun, C.H., and Han, S.H. 2020a. Enhanced biofilm formation of Streptococcus gordonii with lipoprotein deficiency. Mol. Oral Microbiol. 35, 271–278.

    Article  CAS  PubMed  Google Scholar 

  • Park, O.J., Kwon, Y., Park, C., So, Y.J., Park, T.H., Jeong, S., Im, J., Yun, C.H., and Han, S.H. 2020b. Streptococcus gordonii: pathogenesis and host response to its cell wall components. Microorganisms 8, 1852.

    Article  CAS  PubMed Central  Google Scholar 

  • Parks, T., Barrett, L., and Jones, N. 2015. Invasive streptococcal disease: a review for clinicians. Br. Med. Bull. 115, 77–89.

    Article  PubMed  Google Scholar 

  • Preda, V.G. and Săndulescu, O. 2019. Communication is the key: biofilms, quorum sensing, formation and prevention. Discoveries 7, e100.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rice, K.C., Mann, E.E., Endres, J.L., Weiss, E.C., Cassat, J.E., Smeltzer, M.S., and Bayles, K.W. 2007. The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus. Proc. Natl. Acad. Sci. USA 104, 8113–8118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ricker, A., Vickerman, M., and Dongari-Bagtzoglou, A. 2014. Streptococcus gordonii glucosyltransferase promotes biofilm interactions with Candida albicans. J. Oral Microbiol. 6, 23419.

    Article  Google Scholar 

  • Ryu, E.J., Sim, J., Sim, J., Lee, J., and Choi, B.K. 2016. D-Galactose as an autoinducer 2 inhibitor to control the biofilm formation of periodontopathogens. J. Microbiol. 54, 632–637.

    Article  CAS  PubMed  Google Scholar 

  • Song, J., Jung, K.J., Yang, M.J., Han, S.C., and Lee, K. 2021. Assessment of acute and repeated pulmonary toxicities of oligo(2-(2-ethoxy)ethoxyethyl guanidium chloride in mice. Toxicol. Res. 37, 99–113.

    Article  CAS  PubMed  Google Scholar 

  • Stewart, P.S. 2015. Antimicrobial tolerance in biofilms. Microbiol. Spectr. 3. doi: https://doi.org/10.1128/microbiolspec.MB-0010-2014

  • Suzuki, I., Shimizu, T., and Senpuku, H. 2020. Short chain fatty acids induced the type 1 and type 2 fimbrillin-dependent and fimbrillin-independent initial attachment and colonization of Actinomyces oris monoculture but not coculture with streptococci. BMC Microbiol. 20, 329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawre, M.S., Kamble, E.E., Kumkar, S.N., Mulani, M.S., and Pardesi, K.R. 2021. Antibiofilm and antipersister activity of acetic acid against extensively drug resistant Pseudomonas aeruginosa PAW1. PLoS ONE 16, e0246020.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thurlow, L.R., Hanke, M.L., Fritz, T., Angle, A., Aldrich, A., Williams, S.H., Engebretsen, I.L., Bayles, K.W., Horswill, A.R., and Kielian, T. 2011. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol. 186, 6585–6596.

    Article  CAS  PubMed  Google Scholar 

  • Top**, D.L. and Clifton, P.M. 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81, 1031–1064.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Li, X., and Ling, J. 2017. Streptococcus gordonii LuxS/autoinducer-2 quorum-sensing system modulates the dual-species biofilm formation with Streptococcus mutans. J. Basic Microbiol. 57, 605–616.

    Article  CAS  PubMed  Google Scholar 

  • Yombi, J., Belkhir, L., Jonckheere, S., Wilmes, D., Cornu, O., Vandercam, B., and Rodriguez-Villalobos, H. 2012. Streptococcus gordonii septic arthritis: two cases and review of literature. BMC Infect. Dis. 12, 215.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zandi, H., Kristoffersen, A.K., Ørstavik, D., Rôças, I.N., Siqueira, J.F.Jr., and Enersen, M. 2018. Microbial analysis of endodontic infections in root-filled teeth with apical periodontitis before and after irrigation using pyrosequencing. J. Endod. 44, 372–378.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the grants from the National Research Foundation (NRF) funded by the Korean government (NRF-2018R1A5A2024418 and NRF-2019R1A2C2007041).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seung Hyun Han.

Ethics declarations

The authors have no conflicts of interest relevant to this study to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Park, T., Im, J., Kim, A.R. et al. Short-chain fatty acids inhibit the biofilm formation of Streptococcus gordonii through negative regulation of competence-stimulating peptide signaling pathway. J Microbiol. 59, 1142–1149 (2021). https://doi.org/10.1007/s12275-021-1576-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-021-1576-8

Keywords

Navigation