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Evaluation of Human Dental Plaque Lactic Acid Bacilli for Probiotic Potential and Functional Analysis in Relevance to Oral Health

  • ORIGINAL RESEARCH ARTICLE
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Abstract

Members of the lactic acid bacillus group are well-known probiotics and primarily isolated from fermented food, dairy products, intestinal and gut environment of human. Since probiotics from the human source are preferred, there exists a huge repertoire of lactobacilli in the human oral cavity which could prove a much better niche to be exploited for these beneficial microorganisms. Therefore, in this study, four lactobacilli strains, including strain DISK7, reported earlier, isolated from dental plaque samples of a healthy humans were evaluated for their probiotic potential. Strains displayed 99.9% of 16S rRNA gene sequence identity with species of the genera Lactobacillus and Limosilactobacillus. All strains showed lactic acid production, tolerance to low pH and antibiotic sensitivity. Variations were observed among strains in their aggregation ability, biofilm formation, bile salt resistance and cholesterol degradation. Further, we analyzed the interaction of strains with other oral commensals and opportunistic pathogens in co-culture experiments. Isolates DISK7 and DISK26 exhibited high co-aggregation (> 70%) with secondary colonizers, Streptococcus pyogenes and Veillonella parvula, respectively, but their aggregation ability was decreased with opportunistic pathogens. Furthermore, strains showed a substantial increase in biofilm in co-culture with other Lactobacillus isolates, indicating their ability to proliferate commensal bacteria in the oral environment. These microbes continually evolve in terms of niche adaptation as evidenced in genome analysis. The highlight of the investigation is the isolation and evaluation of the probiotic lactobacilli from the human oral cavity, which could prove a much better niche to be exploited for the effective commercialization of these beneficial microbes. Taken together, probiotic properties and interaction with commensal bacteria, these isolates exhibit the huge potential to be developed as alternative bioresource agents for maintenance of oral health.

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Data Availability

16S rRNA gene was submitted to EMBL with accession Nos. for DISK12, DISK16 and DISK26 were OP728783, OP729196 and OP729175, respectively. Whole genome sequences of all strains were submitted to NCBI and available with accession numbers Accession nos., DISK12, MKXG01000001.1; DISK16, MJER01000001.1; DISK26, MJES01000001.1.

References

  1. Tsuda H, Miyamoto T (2010) Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food, 2002. Food Sci Technol Res 16:87–92

    Article  CAS  Google Scholar 

  2. Pereira DI, Gibson GR (2002) Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol 68:4689–4693. https://doi.org/10.1128/AEM.68.9.4689-4693.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Singh SS, Akhtar M, Sharma D, Mandal SM, Korpole S (2021) Characterization of iturin V, a novel antimicrobial lipopeptide from a potential probiotic strain Lactobacillus sp. M31. Probiot Antimicrob Prot 13:1766–1779. https://doi.org/10.1007/s12602-021-09796-2

    Article  CAS  Google Scholar 

  4. Hudault S, Liévin V, Bernet-Camard MF, Servin AL (1997) Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. Appl Environ Microbiol 63:513–518. https://doi.org/10.1128/aem.63.2.513-518.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Pino A, Bartolo E, Caggia C, Cianci A, Randazzo CL (2019) Detection of vaginal lactobacilli as probiotic candidates. Sci Rep 9:1. https://doi.org/10.1038/s41598-019-40304-3

    Article  CAS  Google Scholar 

  6. Sornplang P, Piyadeatsoontorn S (2016) Probiotic isolates from unconventional sources: a review. J Anim Sci Technol 58:1–1. https://doi.org/10.1186/s40781-016-0108-2

    Article  CAS  Google Scholar 

  7. Zheng J, Wittouck S, Salvetti E, Franz CM, Harris HM, Mattarelli P, Otoole PW, Pot B, Vandamme P, Walter J, Watanabe K (2020) A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107

    Article  CAS  PubMed  Google Scholar 

  8. Walter J (2008) Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl Environ Microbiol 74:4985–4996. https://doi.org/10.1128/AEM.00753-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Caufield PW, Schön CN, Saraithong P, Li Y, Argimón S (2015) Oral lactobacilli and dental caries: a model for niche adaptation in humans. J Dent Res 94:110S-S118. https://doi.org/10.1177/0022034515576052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kim JA, Bayo J, Cha J, Choi YJ, Jung MY, Kim DH, Kim Y (2019) Investigating the probiotic characteristics of four microbial strains with potential application in feed industry. PLoS ONE 14:e0218922. https://doi.org/10.1371/journal.pone.0218922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Urvashi SD, Sharma S, Pal V, Lal R, Patil P, Grover V, Korpole S (2020) Bacterial populations in subgingival plaque under healthy and diseased conditions: genomic insights into oral adaptation strategies by Lactobacillus sp. strain DISK7. Indian J Microbiol 60:78–86. https://doi.org/10.1007/s12088-019-00828-8

    Article  CAS  PubMed  Google Scholar 

  12. Nallabelli N, Patil PP, Pal VK, Singh N, Jain A, Patil PB, Korpole GV, S, (2016) Biochemical and genome sequence analyses of Megasphaera sp. strain DISK18 from dental plaque of a healthy individual reveal’s commensal lifestyle. Sci Rep 6:1–3. https://doi.org/10.1038/srep33665

    Article  CAS  Google Scholar 

  13. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci 106:19126–19131. https://doi.org/10.1073/pnas.0906412106

    Article  PubMed  PubMed Central  Google Scholar 

  14. Malik A, Sakamoto M, Hanazaki S, Osawa M, Suzuki T, Tochigi M, Kakii K (2003) Coaggregation among nonflocculating bacteria isolated from activated sludge. Appl Environ Microbiol 69:6056–6063. https://doi.org/10.1128/AEM.69.10.6056-6063.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kumar R, Grover S, Batish VK (2012) Bile salt hydrolase (Bsh) activity screening of Lactobacilli: in vitro selection of indigenous Lactobacillus strains with potential bile salt hydrolysing and cholesterol-lowering ability. Probiot Antimicrob Prot 4:162–172. https://doi.org/10.1007/s12602-012-9101-3

    Article  CAS  Google Scholar 

  16. Gilliland SE, Nelson CR, Maxwell C (1985) Assimilation of cholesterol by Lactobacillus acidophilus. Appl Environ Microbiol 49:377–381. https://doi.org/10.1128/aem.49.2.377-381.1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Koul S, Kalia VC (2016) Comparative genomics reveals biomarkers to identify Lactobacillus species. Indian J Microbiol 56:265–276. https://doi.org/10.1007/s12088-016-0605-5

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kalia VC, Kumar R, Kumar P, Koul S (2016) A genome-wide profiling strategy as an aid for searching unique identification biomarkers for Streptococcus. Indian J Microbiol 56:46–58. https://doi.org/10.1007/s12088-015-0561-5

    Article  CAS  PubMed  Google Scholar 

  19. Tanizawa Y, Tada I, Kobayashi H, Endo A, Maeno S, Toyoda A, Arita M, Nakamura Y, Sakamoto M, Ohkuma M, Tohno M (2018) Lactobacillus paragasseri sp. nov., a sister taxon of Lactobacillus gasseri, based on whole-genome sequence analyses. Int J Syst Evol Microbiol 68:3512–3517. https://doi.org/10.1099/ijsem.0.003020

    Article  CAS  PubMed  Google Scholar 

  20. Cornejo OE, Lefébure T, Bitar PD, Lang P, Richards VP, Eilertson K, Do T, Beighton D, Zeng L, Ahn SJ, Burne RA, Siepel A, Bustamante CD, Stanhope MJ (2013) Evolutionary and population genomics of the cavity causing bacteria Streptococcus mutans. Mol Biol Evol 30:881–93. https://doi.org/10.1093/molbev/mss278

    Article  CAS  PubMed  Google Scholar 

  21. Kalia VC, Raju SC, Purohit HJ (2011) Genomic analysis reveals versatile organisms for quorum quenching enzymes: acyl-homoserine lactone-acylase and -lactonase. Open Microbiol J 5:1–13. https://doi.org/10.2174/1874285801105010001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Colombo AP, do Souto RM, da Silva-Boghossian CM, Miranda R, Lourenço TG (2015) Microbiology of oral biofilm-dependent diseases: have we made significant progress to understand and treat these diseases? Curr Oral Health Rep 2:37–47. https://doi.org/10.1007/s40496-014-0041-8

    Article  Google Scholar 

  23. Mäkeläinen H, Hasselwander O, Rautonen N, Ouwehand AC (200) Panose, a new prebiotic candidate. Lett Appl Microbiol 49:666–672

  24. Ventura M, Turroni F, Zomer A, Foroni E, Giubellini V, Bottacini F, Canchaya C, Claesson MJ, He F, Mantzourani M, Mulas L (2009) The Bifidobacterium dentium Bd1 genome sequence reflects its genetic adaptation to the human oral cavity. PLoS Genet 5:e1000785. https://doi.org/10.1371/journal.pgen.1000785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mendes-Soares H, Suzuki H, Hickey RJ, Forney LJ (2014) Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J Bacteriol 196:1458–1470. https://doi.org/10.1128/JB.01439-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Broadbent JR, Neeno-Eckwall EC, Stahl B, Tandee K, Cai H, Morovic W, Horvath P, Heidenreich J, Perna NT, Barrangou R, Steele JL (2012) Analysis of the Lactobacillus casei supragenome and its influence in species evolution and lifestyle adaptation. BMC Genom 13:1–8. https://doi.org/10.1186/1471-2164-13-533

    Article  CAS  Google Scholar 

  27. Sabir F, Beyatli Y, Cokmus C, Onal-Darilmaz D (2010) Assessment of potential probiotic properties of Lactobacillus spp., Lactococcus spp., and Pediococcus spp. strains isolated from kefir. J Food Sci 75:M568–M573. https://doi.org/10.1111/j.1750-3841.2010.01855.x

    Article  CAS  PubMed  Google Scholar 

  28. Yadav AS, Kolluri G, Gopi M, Karthik K, Malik Y, Dharma K (2016) Exploring alternatives to antibiotics as health promoting agents in poultry-a review. J Exp Biol 4:368–383. https://doi.org/10.18006/2016.4(3S).368.383

    Article  Google Scholar 

  29. Zhu L, Kreth J (2012) The role of hydrogen peroxide in environmental adaptation of oral microbial communities. Oxid Med Cell Longev 2012:717843. https://doi.org/10.1155/2012/717843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ferreira CL, Grześkowiak Ł, Collado MC, Salminen S (2011) In vitro evaluation of Lactobacillus gasseri strains of infant origin on adhesion and aggregation of specific pathogens. J Food Prot 9:1482–7. https://doi.org/10.4315/0362-028X.JFP-11-074

    Article  Google Scholar 

  31. Ocaña VS, Nader-Macías ME (2002) Vaginal lactobacilli: self-and co-aggregating ability. Br J Biomed Sci 59:183–190. https://doi.org/10.1080/09674845.2002.11783657

    Article  PubMed  Google Scholar 

  32. Kolenbrander PE, Andersen RN, Holdeman LV (1985) Co-aggregation of oral Bacteroides species with other bacteria: central role in coaggregation bridges and competitions. Infect Immun 48:741–746. https://doi.org/10.1128/iai.48.3.741-746.1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Takahashi N (2015) Oral microbiome metabolism: From “who are they?” to “what are they doing?” J Dent Res 94:1628–1637. https://doi.org/10.1177/0022034515606045

    Article  CAS  PubMed  Google Scholar 

  34. Kalia VC, Wood TK, Kumar P (2014) Evolution of resistance to quorum-sensing inhibitors. Microbial Ecol 68:13–23. https://doi.org/10.1007/s00248-013-0316-y

    Article  CAS  Google Scholar 

  35. Angelin J, Kavitha M (2020) Exopolysaccharides from probiotic bacteria and their health potential. Int J Biol Macromol 162:853–865. https://doi.org/10.1016/j.ijbiomac.2020.06.190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Koul S, Prakash J, Mishra A, Kalia VC (2016) Potential emergence of multi-quorum sensing inhibitor resistant (MQSIR) bacteria. Ind J Microbiol 56:1–8. https://doi.org/10.1007/s12088-015-0558-0

    Article  CAS  Google Scholar 

  37. Aoudia N, Rieu A, Briandet R, Deschamps J, Chluba J, Jego G, Garrido C, Guzzo J (2016) Biofilms of Lactobacillus plantarum and Lactobacillus fermentum: Effect on stress responses, antagonistic effects on pathogen growth and immunomodulatory properties. Food Microbiol 53:51–59. https://doi.org/10.1016/j.fm.2015.04.009

    Article  CAS  PubMed  Google Scholar 

  38. Sharma P, Tomar SK, Sangwan V, Goswami P, Singh R (2016) Antibiotic resistance of Lactobacillus sp. isolated from commercial probiotic preparations. J Food Saf 36:38–51. https://doi.org/10.1111/jfs.12211

    Article  CAS  Google Scholar 

  39. Jose NM, Bunt CR, Hussain MA (2015) Implications of antibiotic resistance in probiotics. Food Rev Int 31:52–62. https://doi.org/10.1080/87559129.2014.961075

    Article  CAS  Google Scholar 

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Acknowledgements

The financial research support grant was issued by SERB-DST, Department of Science and Technology and Council of Scientific and Industrial Research, Govt of India. CSIR fellowship to Stanzin Choksket and Harshvardhan is duly acknowledged.

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Authors and Affiliations

  1. CSIR-Institute of Microbial Technology, Sector 39A, Chandigarh, India

    Stanzin Choksket, Shikha Sharma,  Harshvardhan, Vijay Pal, Prabhu B. Patil & Suresh Korpole

  2. Dr. Harvansh Singh Judge Institute of Dental Sciences and Hospital, Panjab University, Chandigarh, India

    Ashish Jain & Vishakha Grover

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Contributions

SC, SS, SK and VG were involved in conceptualization. SC, SS, HV, VP, AJ, SK and VG were involved in designing and performing experiments. SS and PBP were involved in the genome sequencing. SC, SS, PBP, SK and VG were involved in data analysis. SC, SS, SK and VG were involved in writing the manuscript.

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Correspondence to Suresh Korpole or Vishakha Grover.

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Choksket, S., Sharma, S., Harshvardhan et al. Evaluation of Human Dental Plaque Lactic Acid Bacilli for Probiotic Potential and Functional Analysis in Relevance to Oral Health. Indian J Microbiol 63, 520–532 (2023). https://doi.org/10.1007/s12088-023-01108-2

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