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Streptococcus mutans and Candida albicans Biofilm Inhibitors Produced by Lactiplantibacillus plantarum CCFM8724

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Abstract

Lactiplantibacillus plantarum CCFM8724 inhibits the growth of Streptococcus mutans and Candida albicans in mixed-species biofilm formation. In this study, bioactive compound including cyclo (leu-pro), cyclo (phe-pro), and some organic acids, such as 3-phenyllactic acid, hydrocinnamic acid, and palmitic acid, were identified through GC–MS analysis. At 50 μg·mL−1, cyclo (leu-pro) reduced biofilm mass (OD600) from 3.00 to 2.00, and hydrocinnamic acid at 25 μg·mL−1 reduced biofilm mass (OD600) from 3.00 to 1.00. The expression of ALS3 and HWP1 was downregulated by cyclo (leu-pro). Furthermore, a mixture of cyclo (leu-pro), cyclo (phe-pro), 3-phenyllactic acid, hydrocinnamic acid, and palmitic acid, had anti-biofilm activity. Overall, the results provide promising baseline information for the potential use of this probiotic and its components in preventing biofilm formation.

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Data Availability

Data used to support the findings of this study are available from the corresponding author upon request.

References

  1. Mitrakul K, Srisatjaluk R, Srisukh V et al (2018) Cymbopogon citratus (Lemongrass Oil) oral sprays as inhibitors of Mutans Streptococci biofilm formation. J Clin Diagn Res. https://doi.org/10.7860/Jcdr/2018/37459.12342

    Article  Google Scholar 

  2. Cugini C, Shanmugam M, Landge N et al (2019) The role of exopolysaccharides in oral biofilms. J Dent Res 98(7):739–745. https://doi.org/10.1177/0022034519845001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Du Q, Ren B, He JZ et al (2020) Candida albicans promotes tooth decay by inducing oral microbial dysbiosis. ISME J 15:894–908. https://doi.org/10.1038/s41396-020-00823-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Yuan KY, Hou LL, Jin QQ et al (2021) Comparative transcriptomics analysis of Streptococcus mutans with disruption of LuxS/AI-2 quorum sensing and recovery of methyl cycle. Arch Oral Biol 127:105137. https://doi.org/10.1016/j.archoralbio.2021.105137

    Article  CAS  PubMed  Google Scholar 

  5. Liu QJ, Wang JF, Ren HQ (2021) Bacterial assembly and succession in the start-up phase of an IFAS metacommunity: the role of AHL-driven quorum sensing. Sci Total Environ 777:145870. https://doi.org/10.1016/j.scitotenv.2021.145870

    Article  CAS  PubMed  Google Scholar 

  6. Li HJ, Liu L, Zhang SW et al (2012) Identification of antifungal compounds produced by Lactobacillus casei AST18. Curr Microbiol 65(2):156–161. https://doi.org/10.1007/s00284-012-0135-2

    Article  CAS  PubMed  Google Scholar 

  7. Li JR, Wang WL, Xu SX et al (2011) Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc Natl Acad Sci USA 108(8):3360–3365. https://doi.org/10.1073/pnas.1017431108

    Article  PubMed  PubMed Central  Google Scholar 

  8. Strom K, Sjogren J, Broberg A et al (2002) Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microb 68(9):4322–4327. https://doi.org/10.1128/Aem.68.9.4322-4327.2002

    Article  CAS  Google Scholar 

  9. Wang CJ, Chang T, Yang H et al (2015) Antibacterial mechanism of lactic acid on physiological and morphological properties of Salmonella Enteritidis, Escherichia coli and Listeria monocytogenes. Food Control 47:231–236. https://doi.org/10.1016/j.foodcont.2014.06.034

    Article  CAS  Google Scholar 

  10. Muench DF, Kuch DJ, Wu H et al (2009) Hydrogen peroxide-producing Lactobacilli inhibit gonococci in vitro but not during experimental genital tract infection. J Infect Dis 199(9):1369–1378. https://doi.org/10.1086/597390

    Article  CAS  PubMed  Google Scholar 

  11. Zou J, Jiang H, Cheng H et al (2018) Strategies for screening, purification and characterization of bacteriocins. Int J Biol Macromol 117:781–789. https://doi.org/10.1016/j.ijbiomac.2018.05.233

    Article  CAS  PubMed  Google Scholar 

  12. Rishi L, Mittal G, Agarwal RK et al (2017) Melioration in anti-staphylococcal activity of conventional antibiotic(s) by organic acids present in the cell free supernatant of Lactobacillus paraplantarum. Indian J Microbiol 57(3):359–364. https://doi.org/10.1007/s12088-017-0659-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Qin S, Xu W, Zhang Q et al (2020) Inhibitory effect of Lactobacillus plantarum CCFM8724 on caries-causing dual biofilms. Food Ferment Indus 46(13):127–132

    Google Scholar 

  14. Zhang QX, Qin SJ, Xu XY et al (2020) Inhibitory effect of Lactobacillus plantarum CCFM8724 towards Streptococcus mutans- and Candida albicans-induced caries in rats. Oxid Med Cell Longev. https://doi.org/10.1155/2020/4345804

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chang CY, Pan TM (2019) Identification of bioactive compounds in Lactobacillus paracasei subsp. paracasei NTU 101-fermented reconstituted skimmed milk and their anti-cancer effect in combination with 5-fluorouracil on colorectal cancer cells. Food Funct 10(12):7634–7644. https://doi.org/10.1039/c9fo01819k

    Article  CAS  PubMed  Google Scholar 

  16. Hasan S, Danishuddin M, Khan AU (2015) Inhibitory effect of zingiber officinale towards Streptococcus mutans virulence and caries development: in vitro and in vivo studies. Bmc Microbiol. https://doi.org/10.1186/s12866-014-0320-5

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lu HQ, Chen HQ, Tang X et al (2019) Evaluation of metabolome sample preparation and extraction methodologies for oleaginous filamentous fungi Mortierella alpina. Metabolomics. https://doi.org/10.1007/s11306-019-1506-5

    Article  PubMed  Google Scholar 

  18. Gowrishankar S, Poornima B, Pandian SK (2014) Inhibitory efficacy of cyclo(L-leucyl-L-prolyl) from mangrove rhizosphere bacterium-Bacillus amyloliquefaciens (MMS-50) toward cariogenic properties of Streptococcus mutans. Res Microbiol 165(4):278–289. https://doi.org/10.1016/j.resmic.2014.03.004

    Article  CAS  PubMed  Google Scholar 

  19. Zhang QX, Li JX, Lu WW et al (2021) Multi-omics reveals the inhibition of Lactiplantibacillus plantarum CCFM8724 in Streptococcus mutans-Candida albicans mixed-species biofilms. Microorganisms 9(11):2368. https://doi.org/10.3390/microorganisms9112368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Li JX, Zhang QX, Guo M et al (2021) Identification of metabolites secreted by Lactobacillus plantarum CCFM8724 on inhibiting dual-species biofilm. Microbiol China 48(12):4719–4730. https://doi.org/10.13344/j.microbiol.china.210458

    Article  CAS  Google Scholar 

  21. Simon G, Berube C, Voyer N et al (2019) Anti-biofilm and anti-adherence properties of novel cyclic dipeptides against oral pathogens. Bioorgan Med Chem 27(12):2323–2331. https://doi.org/10.1016/j.bmc.2018.11.042

    Article  CAS  Google Scholar 

  22. Mashima I, Miyakawa H, Scannapieco FA et al (2018) Identification of an early stage biofilm inhibitor from Veillonella tobetsuensis. Anaerobe 52:86–91. https://doi.org/10.1016/j.anaerobe.2018.06.005

    Article  CAS  PubMed  Google Scholar 

  23. Marchesan JT, Morelli T, Moss K et al (2015) Association of synergistetes and cyclodipeptides with periodontitis. J Dent Res 94(10):1425–1431. https://doi.org/10.1177/0022034515594779

    Article  CAS  PubMed  Google Scholar 

  24. Salehi R, Tahmourespour A, Eslami G (2009) The effects of some probiotics on Gtfb and Gtfc gene expression levels in biofilm producing S. Mutans by real-time Rt-Pcr Iubmb. Life 61(3):310–310

    Google Scholar 

  25. Hung DCI, Downey JS, Ayala EA et al (2011) Characterization of DNA Binding Sites of the ComE response regulator from Streptococcus mutans. J Bacteriol 193(14):3642–3652. https://doi.org/10.1128/Jb.00155-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Fan Y, He H, Dong Y et al (2013) Hyphae-specific genes HGC1, ALS3, HWP1, and ECE1 and relevant signaling pathways in Candida albicans. Mycopathologia 176(5–6):329–335. https://doi.org/10.1007/s11046-013-9684-6

    Article  CAS  PubMed  Google Scholar 

  27. Maiti P, Ghorai P, Ghosh S et al (2015) Mapping of functional domains and characterization of the transcription factor Cph1 that mediate morphogenesis in Candida albicans. Fungal Genet Biol 83:45–57. https://doi.org/10.1016/j.fgb.2015.08.004

    Article  CAS  PubMed  Google Scholar 

  28. Mun SY, Kim SK, Woo ER et al (2019) Purification and characterization of an antimicrobial compound produced by Lactobacillus plantarum EM showing both antifungal and antibacterial activities. Lwt-Food Sci Technol. 114:108403. https://doi.org/10.1016/j.lwt.2019.108403

    Article  CAS  Google Scholar 

  29. Dal Bello F, Clarke CI, Ryan LAM et al (2007) Improvement of the quality and shelf life of wheat bread by fermentation with the antifungal strain Lactobacillus plantarum FST 1.7. J Cereal Sci 45(3):309–318. https://doi.org/10.1016/j.jcs.2006.09.004

    Article  CAS  Google Scholar 

  30. Rodriguez N, Salgado JM, Cortes S et al (2012) Antimicrobial activity of D-3-phenyllactic acid produced by fed-batch process against Salmonella enterica. Food Control 25(1):274–284. https://doi.org/10.1016/j.foodcont.2011.10.042

  31. Sharma S, Gopu V, Sivasankar C et al (2019) Hydrocinnamic acid produced by Enterobacter xiangfangensis impairs AHL-based quorum sensing and biofilm formation in Pseudomonas aeruginosa. Rsc Adv 9(49):28678–28687. https://doi.org/10.1039/c9ra05725k

    Article  CAS  Google Scholar 

  32. Prasath KG, Tharani H, Kumar MS et al (2020) Palmitic acid inhibits the virulence factors of Candida tropicalis: biofilms, cell surface hydrophobicity, ergosterol biosynthesis, and enzymatic activity. Front Microbiol. https://doi.org/10.3389/fmicb.2020.00864

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ding T, Li Y (2020) Inhibition on quorum sensing of Pseudomonas fluorescens by cyclic dipeptide isolated from Aspergillus oryzae and its mechanism. Chin J Bioprocess Eng 18(2):234–244

    Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant Nos. 32072197, 32021005), National First-class Discipline Program of Food Science and Technology (Grant No. JUFSTR20180102), and Collaborative innovation center of food safety and quality control in Jiangsu Province.

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China

    Jiaxun Li, Qiuxiang Zhang, Jianxin Zhao, Hao Zhang & Wei Chen

  2. School of Food Science and Technology, Jiangnan University, Wuxi, 214122, Jiangsu, China

    Jiaxun Li, Qiuxiang Zhang, Jianxin Zhao, Hao Zhang & Wei Chen

  3. (Yangzhou) Institute of Food Biotechnology, Jiangnan University, Yangzhou, 225004, China

    Qiuxiang Zhang

  4. National Engineering Research Center for Functional Food, Jiangnan University, Wuxi, 214122, Jiangsu, China

    Hao Zhang & Wei Chen

Authors
  1. Jiaxun Li
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  2. Qiuxiang Zhang
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  3. Jianxin Zhao
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  4. Hao Zhang
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  5. Wei Chen
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Contributions

JL: Contributed to conception, design, data acquisition, analysis and interpretation, drafted and critically revised the manuscript. QZ: Contributed to conception, design, analysis, critically revised the manuscript. JZ, HZ, WC: Contributed to conception and critically revised the manuscript. All authors gave their final approval and agree to be accountable for all aspects of the work.

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Correspondence to Qiuxiang Zhang.

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Li, J., Zhang, Q., Zhao, J. et al. Streptococcus mutans and Candida albicans Biofilm Inhibitors Produced by Lactiplantibacillus plantarum CCFM8724. Curr Microbiol 79, 143 (2022). https://doi.org/10.1007/s00284-022-02833-5

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