Exploration of the Main Antibiofilm Substance of Lactobacillus plantarum ATCC 14917 and Its Effect against Streptococcus mutans

Dental plaque, a complex biofilm system established by cariogenic bacteria such as Streptococcus mutans (S. mutans), is the initiator of dental caries. Studies have found that the cell-free supernatant (CFS) of Lactobacilli could inhibit S. mutans biofilm formation. However, the main antibiofilm substance of the Lactobacilli CFS that acts against S. mutans is unclear. The present study found that the CFS of Lactobacillus plantarum (L. plantarum) ATCC 14917 had the strongest antibiofilm effect among the five tested oral Lactobacilli. Further bioassay-guided isolation was performed to identify the main antibiofilm substance. The antibiofilm effect of the end product, named 1-1-4-3, was observed and the structure of it was elucidated by using Q-TOF MS, 2D NMR and HPLC. The results showed that several components in the CFS had an antibiofilm effect; however, the effect of 1-1-4-3 was the strongest, as it could reduce the generation of exopolysaccharides and make the biofilm looser and thinner. After structure elucidation and validation, 1-1-4-3 was identified as a mixture of lactic acid (LA) and valine. Additionally, LA was shown to be the main antibiofilm substance in 1-1-4-3. In summary, this study found that the antibiofilm effect of the L. plantarum CFS against S. mutans was attributable to the comprehensive effect of multiple components, among which LA played a dominant role.

[1]  Isaac Duah Boateng Evaluating the status quo of deep eutectic solvent in food chemistry. Potentials and limitations. , 2022, Food chemistry.

[2]  Qun Sun,et al.  Acetylation of Lactate Dehydrogenase Negatively Regulates the Acidogenicity of Streptococcus mutans , 2022, mBio.

[3]  V. Casolaro,et al.  Rhein: A novel antibacterial compound against Streptococcus mutans infection. , 2022, Microbiological research.

[4]  Xiaoge Jiang,et al.  Inhibition of Streptococcus mutans Biofilm Formation by the Joint Action of Oxyresveratrol and Lactobacillus casei , 2022, Applied and environmental microbiology.

[5]  A. López‐Malo,et al.  The impacts of antimicrobial and antifungal activity of cell‐free supernatants from lactic acid bacteria in vitro and foods , 2021, Comprehensive Reviews in Food Science and Food Safety.

[6]  Yuqi Cui,et al.  Small molecule targeting amyloid fibrils inhibits Streptococcus mutans biofilm formation , 2021, AMB Express.

[7]  Ya-Ping Liu,et al.  Alstoscholarisine K, an Antimicrobial Indole from Gall-Induced Leaves of Alstonia scholaris. , 2021, Organic letters.

[8]  R. Brüschweiler,et al.  2D NMR-Based Metabolomics with HSQC/TOCSY NOAH Supersequences. , 2021, Analytical chemistry.

[9]  K. Yang,et al.  Lactobacillus reuteri AN417 cell-free culture supernatant as a novel antibacterial agent targeting oral pathogenic bacteria , 2021, Scientific reports.

[10]  M. Belleville,et al.  Membrane Fractionation of Protein Hydrolysates from By-Products: Recovery of Valuable Compounds from Spent Yeasts , 2020, Membranes.

[11]  L. Dicks,et al.  Molecular insights into probiotic mechanisms of action employed against intestinal pathogenic bacteria , 2020, Gut microbes.

[12]  Yina Cao,et al.  Proteomic and metabolic characterization of membrane vesicles derived from Streptococcus mutans at different pH values , 2020, Applied Microbiology and Biotechnology.

[13]  S. Krisanaprakornkit,et al.  Significant elevation of salivary human neutrophil peptides 1-3 levels by probiotic milk in preschool children with severe early childhood caries: a randomized controlled trial , 2020, Clinical Oral Investigations.

[14]  Jesús Martín,et al.  Strasseriolides A-D, A Family of Antiplasmodial Macrolides Isolated from the Fungus Strasseria geniculata CF-247251. , 2020, Organic letters.

[15]  B. Sivamaruthi,et al.  A Review of the Role of Probiotic Supplementation in Dental Caries , 2020, Probiotics and Antimicrobial Proteins.

[16]  R. Nomura,et al.  Oral Lactobacilli Related to Caries Status of Children with Primary Dentition , 2020, Caries Research.

[17]  Yu-ting Su,et al.  Antimicrobial ability and mechanism analysis of Lactobacillus species against carbapenemase-producing Enterobacteriaceae. , 2020, Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi.

[18]  Jinpeng Wang,et al.  Antibacterial activity of a polysaccharide produced from Chaetomium globosum CGMCC 6882. , 2019, International journal of biological macromolecules.

[19]  Tao Zhang,et al.  Isocoumarindole A, a Chlorinated Isocoumarin and Indole Alkaloid Hybrid Metabolite from an Endolichenic Fungus Aspergillus sp. , 2019, Organic letters.

[20]  G. Du,et al.  Characterization of a Lactobacillus brevis strain with potential oral probiotic properties , 2018, BMC Microbiology.

[21]  A. McBain,et al.  Oral Microbiota in Severe Early Childhood Caries in Thai Children and Their Families: A Pilot Study , 2018, Front. Microbiol..

[22]  A. Anbinder,et al.  Inhibitory effect of probiotic Lactobacillus supernatants from the oral cavity on Streptococcus mutans biofilms. , 2018, Microbial pathogenesis.

[23]  K. Seo,et al.  Antimicrobial and anti-biofilm activities of Lactobacillus kefiranofaciens DD2 against oral pathogens , 2018, Journal of oral microbiology.

[24]  T. Vos,et al.  Global, Regional, and National Prevalence, Incidence, and Disability-Adjusted Life Years for Oral Conditions for 195 Countries, 1990–2015: A Systematic Analysis for the Global Burden of Diseases, Injuries, and Risk Factors , 2017, Journal of dental research.

[25]  I. Banat,et al.  Biosurfactants: promising bioactive molecules for oral-related health applications. , 2016, FEMS microbiology letters.

[26]  A. Bytyçi,et al.  Association between salivary level of infection with Streptococcus mutans/Lactobacilli and caries-risk factors in mothers. , 2016, European journal of paediatric dentistry.

[27]  S. Piwat,et al.  Purification and characterization of bacteriocin produced by oral Lactobacillus paracasei SD1. , 2014, Anaerobe.

[28]  M. Xian,et al.  Not only osmoprotectant: betaine increased lactate dehydrogenase activity and L-lactate production in lactobacilli. , 2013, Bioresource technology.

[29]  C. Badet,et al.  Antibacterial activity of probiotic candidates for oral health. , 2013, Anaerobe.

[30]  G. Dahlén,et al.  Inhibitory effect of oral Lactobacillus against oral pathogens , 2011, Letters in applied microbiology.

[31]  H. Harmsen,et al.  Oral Biofilm Architecture on Natural Teeth , 2010, PloS one.

[32]  M. Kojić,et al.  Purification of bacteriocin LS1 produced by human oral isolate Lactobacillus salivarius BGHO1. , 2008, Oral microbiology and immunology.

[33]  J. Gebler,et al.  Orthogonality of separation in two-dimensional liquid chromatography. , 2005, Analytical chemistry.

[34]  T. Watson,et al.  Molecular Analysis of the Microflora Associated with Dental Caries , 2004, Journal of Clinical Microbiology.

[35]  D. Story Bench-to-bedside review: A brief history of clinical acid–base , 2004, Critical care.

[36]  G. Svensäter,et al.  The Acid-Tolerant Microbiota Associated with Plaque from Initial Caries and Healthy Tooth Surfaces , 2003, Caries Research.

[37]  Roberto Kolter,et al.  Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis , 1998, Molecular microbiology.

[38]  S. Assinder,et al.  Inhibition of acid production in Streptococcus mutans R9: inhibition constants and reversibility. , 1995, FEMS microbiology letters.

[39]  J. Giddings Sample dimensionality: a predictor of order-disorder in component peak distribution in multidimensional separation. , 1995, Journal of chromatography. A.

[40]  R. E. Marquis,et al.  Adaptation of Streptococcus mutans and Enterococcus hirae to acid stress in continuous culture , 1991, Applied and environmental microbiology.

[41]  N. Takahashi,et al.  Difference in Amounts between Titratable Acid and Total Carboxylic Acids Produced by Oral Streptococci during Sugar Metabolism , 1989, Journal of dental research.

[42]  H. Chen,et al.  The effect of five probiotic lactobacilli strains on the growth and biofilm formation of Streptococcus mutans. , 2015, Oral diseases.

[43]  Yihong Li,et al.  Oral Lactobacilli and Dental Caries: A Model for Niche Adaptation in Humans CLiNiCAL RevieW , 2015 .