Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Propionate Attenuates Growth of Oral Streptococci through Enhancing Methionine Biosynthesis

  • Park, Taehwan (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Im, Jintaek (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Kim, A Reum (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Lee, Dongwook (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Jeong, Sungho (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University) ;
  • Yun, Cheol-Heui (Department of Agricultural Biotechnology, and Research Institute of Agriculture and Life Sciences, Seoul National University) ;
  • Han, Seung Hyun (Department of Oral Microbiology and Immunology, and Dental Research Institute, School of Dentistry, Seoul National University)
  • Received : 2022.05.22
  • Accepted : 2022.08.30
  • Published : 2022.10.28
Download PDF
⟨ Previous Next ⟩

Abstract

Oral streptococci are considered as an opportunistic pathogen associated with initiation and progression of various oral diseases. However, since the currently-available treatments often accompany adverse effects, alternative strategy is demanded to control streptococci. In the current study, we investigated whether short-chain fatty acids (SCFAs), including sodium acetate (NaA), sodium propionate (NaP), and sodium butyrate (NaB), can inhibit the growth of oral streptococci. Among the tested SCFAs, NaP most potently inhibited the growth of laboratory and clinically isolated strains of Streptococcus gordonii under anaerobic culture conditions. However, the growth inhibitory effect of NaP on six different species of other oral streptococci was different depending on their culture conditions. Metabolic changes such as alteration of methionine biosynthesis can affect bacterial growth. Indeed, NaP enhanced intracellular methionine levels of oral streptococci as well as the mRNA expression level of methionine biosynthesis-related genes. Collectively, these results suggest that NaP has an inhibitory effect on the growth of oral streptococci, which might be due to alteration of methionine biosynthesis. Thus, NaP can be used an effective bacteriostatic agent for the prevention of oral infectious diseases caused by oral streptococci.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (NRF-2018R1A5A2024418, NRF-2019R1A2C2007041, NRF-2022M3A9F3082330, and RS-2022-00164722).

References

  1. Peres MA, Macpherson LMD, Weyant RJ, Daly B, Venturelli R, Mathur MR, et al. 2019. Oral diseases: a global public health challenge. Lancet 394: 249-260. https://doi.org/10.1016/S0140-6736(19)31146-8
  2. Seitz MW, Listl S, Bartols A, Schubert I, Blaschke K, Haux C, et al. 2019. Current knowledge on correlations between highly prevalent dental conditions and chronic diseases: an umbrella review. Prev. Chronic Dis. 16: E132.
  3. Listl S, Galloway J, Mossey PA, Marcenes W. 2015. Global economic impact of dental diseases. J. Dent. Res. 94: 1355-1361. https://doi.org/10.1177/0022034515602879
  4. Rocas IN, Hulsmann M, Siqueira JF, Jr. 2008. Microorganisms in root canal-treated teeth from a German population. J. Endod. 34: 926-931. https://doi.org/10.1016/j.joen.2008.05.008
  5. Vieira AR, Hiller NL, Powell E, Kim LH, Spirk T, Modesto A, et al. 2019. Profiling microorganisms in whole saliva of children with and without dental caries. Clin. Exp. Dent. Res. 5: 438-446. https://doi.org/10.1002/cre2.206
  6. Abranches J, Zeng L, Kajfasz JK, Palmer SR, Chakraborty B, Wen ZT, et al. 2018. Biology of oral streptococci. Microbiol. Spectr. 6: GPP3-0042-2018.
  7. Park OJ, Yi H, Jeon JH, Kang SS, Koo KT, Kum KY, et al. 2015. Pyrosequencing analysis of subgingival microbiota in distinct periodontal conditions. J. Dent. Res. 94: 921-927. https://doi.org/10.1177/0022034515583531
  8. Chavez de Paz L, Svensater G, Dahlen G, Bergenholtz G. 2005. Streptococci from root canals in teeth with apical periodontitis receiving endodontic treatment. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 100: 232-241. https://doi.org/10.1016/j.tripleo.2004.10.008
  9. Kim D, Kim E. 2014. Antimicrobial effect of calcium hydroxide as an intracanal medicament in root canal treatment: a literature review - Part I. In vitro studies. Restor. Dent. Endod. 39: 241-252. https://doi.org/10.5395/rde.2014.39.4.241
  10. Bescos R, Ashworth A, Cutler C, Brookes ZL, Belfield L, Rodiles A, et al. 2020. Effects of chlorhexidine mouthwash on the oral microbiome. Sci. Rep. 10: 5254. https://doi.org/10.1038/s41598-020-61912-4
  11. Addy M, Hunter ML. 2003. Can tooth brushing damage your health? Effects on oral and dental tissues. Int. Dent. J. 53 Suppl 3: 177-186. https://doi.org/10.1111/j.1875-595X.2003.tb00768.x
  12. Brookes ZLS, Bescos R, Belfield LA, Ali K, Roberts A. 2020. Current uses of chlorhexidine for management of oral disease: a narrative review. J. Dent. 103: 103497. https://doi.org/10.1016/j.jdent.2020.103497
  13. Heta S, Robo I. 2018. The side effects of the most commonly used group of antibiotics in periodontal treatments. Med. Sci (Basel). 6: 6.
  14. Moazami F, Sahebi S, Jamshidi D, Alavi A. 2014. The long-term effect of calcium hydroxide, calcium-enriched mixture cement and mineral trioxide aggregate on dentin strength. Iran Endod. J. 9: 185-189.
  15. Topping DL, Clifton PM. 2001. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81: 1031-1064. https://doi.org/10.1152/physrev.2001.81.3.1031
  16. Cummings JH. 1981. Short chain fatty acids in the human colon. Gut 22: 763-779. https://doi.org/10.1136/gut.22.9.763
  17. Lu R, Meng H, Gao X, Xu L, 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. https://doi.org/10.1111/jre.12137
  18. Parada Venegas D, De la Fuente MK, Landskron G, Gonzalez MJ, Quera R, Dijkstra G, et al. 2019. Short chain fatty acids (SCFAs)-mediated gut epithelial and immune regulation and its relevance for inflammatory bowel diseases. Front. Immunol. 10: 277. https://doi.org/10.3389/fimmu.2019.00277
  19. Hojo K, Nagaoka S, Ohshima T, Maeda N. 2009. Bacterial interactions in dental biofilm development. J. Dent. Res. 88: 982-990. https://doi.org/10.1177/0022034509346811
  20. Sim JR, Kang SS, Lee D, Yun CH, Han SH. 2018. Killed whole-cell oral cholera vaccine induces CCL20 secretion by human intestinal epithelial cells in the presence of the short-chain fatty acid, butyrate. Front. Immunol. 9: 55. https://doi.org/10.3389/fimmu.2018.00055
  21. Park JW, Kim HY, Kim MG, Jeong S, Yun CH, Han SH. 2019. Short-chain fatty acids inhibit staphylococcal lipoprotein-induced nitric oxide production in murine macrophages. Immune Netw. 19: e9. https://doi.org/10.4110/in.2019.19.e9
  22. Pinhal S, Ropers D, Geiselmann J, de Jong H. 2019. Acetate metabolism and the inhibition of bacterial growth by acetate. J. Bacteriol. 201: e00147-19.
  23. Yonezawa H, Osaki T, Hanawa T, Kurata S, Zaman C, Woo TDH, et al. 2012. Destructive effects of butyrate on the cell envelope of Helicobacter pylori. J. Med. Microbiol. 61: 582-589. https://doi.org/10.1099/jmm.0.039040-0
  24. Jeong S, Kim HY, Kim AR, Yun CH, Han SH. 2019. Propionate ameliorates Staphylococcus aureus skin infection by attenuating bacterial growth. Front. Microbiol. 10: 1363. https://doi.org/10.3389/fmicb.2019.01363
  25. Jeong S, Lee Y, Yun CH, Park OJ, Han SH. 2019. Propionate, together with triple antibiotics, inhibits the growth of Enterococci. J. Microbiol. 57: 1019-1024. https://doi.org/10.1007/s12275-019-9434-7
  26. Song J, Jung KJ, Yang MJ, Han SC, 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. https://doi.org/10.1007/s43188-020-00058-x
  27. Maruyama K, Kitamura H. 1985. Mechanisms of growth inhibition by propionate and restoration of the growth by sodium bicarbonate or acetate in Rhodopseudomonas sphaeroides S. J. Biochem. 98: 819-824. https://doi.org/10.1093/oxfordjournals.jbchem.a135340
  28. Roe AJ, O'Byrne C, McLaggan D, Booth IR. 2002. Inhibition of Escherichia coli growth by acetic acid: a problem with methionine biosynthesis and homocysteine toxicity. Microbiology (Reading) 148: 2215-2222. https://doi.org/10.1099/00221287-148-7-2215
  29. Ghorbani P, Santhakumar P, Hu Q, Djiadeu P, Wolever TM, Palaniyar N, et al. 2015. Short-chain fatty acids affect cystic fibrosis airway inflammation and bacterial growth. Eur. Respir. J. 46: 1033-1045. https://doi.org/10.1183/09031936.00143614
  30. Sa-Pessoa J, Paiva S, Ribas D, Silva IJ, Viegas SC, Arraiano CM, et al. 2013. SATP (YaaH), a succinate-acetate transporter protein in Escherichia coli. Biochem. J. 454: 585-595. https://doi.org/10.1042/BJ20130412
  31. Jolkver E, Emer D, Ballan S, Kramer R, Eikmanns BJ, 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. https://doi.org/10.1128/JB.01155-08
  32. Hendrickson EL, Wang T, Dickinson BC, Whitmore SE, Wright CJ, Lamont RJ, et al. 2012. Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiol. 12: 211. https://doi.org/10.1186/1471-2180-12-211
  33. Carlsson J, Hamilton IR. 1996. Differential toxic effects of lactate and acetate on the metabolism of Streptococcus mutans and Streptococcus sanguis. Oral Microbiol. Immunol. 11: 412-419. https://doi.org/10.1111/j.1399-302X.1996.tb00204.x
  34. Hartmanis MG. 1987. Butyrate kinase from Clostridium acetobutylicum. J. Biol. Chem. 262: 617-621. https://doi.org/10.1016/S0021-9258(19)75828-1
  35. Savvi S, Warner DF, Kana BD, McKinney JD, Mizrahi V, Dawes SS. 2008. Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J. Bacteriol. 190: 3886-3895. https://doi.org/10.1128/JB.01767-07
  36. Rinehart E, Newton E, Marasco MA, Beemiller K, Zani A, Muratore MK, et al. 2018. Listeria monocytogenes response to propionate is differentially modulated by anaerobicity. Pathogens 7: 60. https://doi.org/10.3390/pathogens7030060
  37. Dong Y, Chen YY, Snyder JA, Burne RA. 2002. Isolation and molecular analysis of the gene cluster for the arginine deiminase system from Streptococcus gordonii DL1. Appl. Environ. Microbiol. 68: 5549-5553. https://doi.org/10.1128/AEM.68.11.5549-5553.2002
  38. Willenborg J, Koczula A, Fulde M, de Greeff A, Beineke A, Eisenreich W, et al. 2016. FlpS, the FNR-like protein of Streptococcus suis is an essential, oxygen-sensing activator of the arginine deiminase system. Pathogens 5: 51. https://doi.org/10.3390/pathogens5030051
  39. Takahashi T, Fujii Y, Takahashi H. 1967. Inhibition of yeast growth by methionine. Agric. Biol. Chem. 31: 664-670.
  40. Johnson CL, Vishniac W. 1970. Growth inhibition in Thiobacillus neapolitanus by histidine, methionine, phenylalanine, and threonine. J. Bacteriol. 104: 1145-1150. https://doi.org/10.1128/jb.104.3.1145-1150.1970
  41. Tuite NL, Fraser KR, O'Byrne C P. 2005. Homocysteine toxicity in Escherichia coli is caused by a perturbation of branched-chain amino acid biosynthesis. J. Bacteriol. 187: 4362-4371. https://doi.org/10.1128/JB.187.13.4362-4371.2005
  42. Afzal M, Shafeeq S, Kuipers OP. 2016. Methionine-mediated gene expression and characterization of the CmhR regulon in Streptococcus pneumoniae. Microb. Genom. 2: e000091.
  43. Kreth J, Merritt J, Qi F. 2009. Bacterial and host interactions of oral streptococci. DNA Cell Biol. 28: 397-403. https://doi.org/10.1089/dna.2009.0868