Skip to main content

Advertisement

Log in

Tapioca Starch Modulates Cellular Events in Oral Probiotic Streptococcus salivarius Strains

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Considering the implications of microbiota in health, scientists are in search of microbiota-oriented strategies for the effective prevention and/or treatment of a wide variety of serious diseases. A microbiota comprises diverse microorganisms with either probiotic or pathogenic properties. The fermentation of prebiotic carbohydrates by probiotic bacteria can affect host metabolism. Therefore, understanding the prebiotic-mediated metabolic modulations in probiotics is crucial to develop functional foods for the improvement of disturbed microbiota. Studies have emphasized the importance of prebiotics in probiotic therapies for mucosal diseases and highlighted the need for extensive research on oral bacteria. In the present study, the cellular events have been studied in batch cultures of probiotic Streptococcus salivarius exposed to the natural prebiotic, tapioca starch (TS). TS modulated the keystone metabolic events in Streptococcus salivarius in a dose-dependent manner. Besides increasing the live cell counts and altering the colony morphologies, TS affected the protein metabolism in terms of cellular expression and conformational changes in protein secondary structures. After treatment with TS, the nucleic acid synthesis increased and B-DNA was more than A- and Z-DNA, together with the diminished fatty acids and increased polysaccharide synthesis. The study results can be considered for the assessment of functional foods and probiotics in oral health.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Bustamante M, Oomah BD, Mosi-Roa Y, et al (2019) Probiotics as an adjunct therapy for the treatment of halitosis, dental caries and periodontitis. Probiotics Antimicrob proteins published online ahead of print, 2019 Feb 7. https://doi.org/10.1007/s12602-019-9521-4

  2. Elshikh M, Marchant R, Banat IM (2016) Biosurfactants: promising bioactive molecules for oral-related health applications. FEMS Microbiol Lett 363:fnw213. https://doi.org/10.1093/femsle/fnw213

    Article  CAS  PubMed  Google Scholar 

  3. Anusha RL, Umar D, Basheer B, Baroudi K (2015) The magic of magic bugs in oral cavity: probiotics. J Adv Pharm Technol Res 6:43–47. https://doi.org/10.4103/2231-4040.154526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lu M, Xuan S, Wang Z (2019) Oral microbiota: a new view of body health. Food Sci Human Wellness 8:8–15. https://doi.org/10.1016/j.fshw.2018.12.001

    Article  Google Scholar 

  5. Lin TH, Lin CH, Pan TM (2018) The implication of probiotics in the prevention of dental caries. Appl Microbiol Biotechnol 102:577–586. https://doi.org/10.1007/s00253-017-8664-z

    Article  CAS  PubMed  Google Scholar 

  6. Nadelman P, Magno MB, Masterson D, da Cruz AG, Maia LC (2018) Are dairy products containing probiotics beneficial for oral health? A systematic review and meta-analysis. Clin Oral Investig 22:2763–2785. https://doi.org/10.1007/s00784-018-2682-9

    Article  PubMed  Google Scholar 

  7. Sajedinejad N, Paknejad M, Houshmand B, Sharafi H, Jelodar R, Shahbani Zahiri H, Noghabi KA (2018) Lactobacillus salivarius NK02: a potent probiotic for clinical application in mouthwash. Probiotics Antimicrob Proteins 10:485–495. https://doi.org/10.1007/s12602-017-9296-4

    Article  CAS  PubMed  Google Scholar 

  8. Riccia DND, Bizzini F, Perilli MG, Polimeni A, Trinchieri V, Amicosante G, Cifone MG (2007) Anti-inflammatory effects of Lactobacillus brevis (CD2) on periodontal disease. Oral Dis 13:376–385. https://doi.org/10.1111/j.1601-0825.2006.01291.x

    Article  PubMed  Google Scholar 

  9. Mahasneh SA, Mahasneh AM (2017) Probiotics: a promising role in dental health. Dent J 5:26. https://doi.org/10.3390/dj5040026

    Article  Google Scholar 

  10. Zhang Y, Wang X, Li H, Ni C, du Z, Yan F (2018) Human oral microbiota and its modulation for oral health. Biomed Pharmacother 99:883–893. https://doi.org/10.1016/j.biopha.2018.01.146

    Article  PubMed  Google Scholar 

  11. Deogade SC (2015) Probiotics: contributions to oral and dental health. J Oral Heal Dent Manag 14:145–154

    Google Scholar 

  12. Wilcox CR, Stuart B, Leaver H, Lown M, Willcox M, Moore M, Little P (2019) Effectiveness of the probiotic Streptococcus salivarius K12 for the treatment and/or prevention of sore throat: a systematic review. Clin Microbiol Infect 25:673–680. https://doi.org/10.1016/j.cmi.2018.12.031

    Article  CAS  PubMed  Google Scholar 

  13. Burton JP, Drummond BK, Chilcott CN, Tagg JR, Thomson WM, Hale JDF, Wescombe PA (2013) Influence of the probiotic Streptococcus salivarius strain M18 on indices of dental health in children: a randomized double-blind, placebo-controlled trial. J Med Microbiol 62:875–884. https://doi.org/10.1099/jmm.0.056663-0

    Article  PubMed  Google Scholar 

  14. Di Pierro F, Zanvit A, Nobili P et al (2015) Cariogram outcome after 90 days of oral treatment with Streptococcus salivarius M18 in children at high risk for dental caries: results of a randomized, controlled study. Clin Cosmet Investig Dent 7:107–113. https://doi.org/10.2147/CCIDE.S93066

    Article  PubMed  PubMed Central  Google Scholar 

  15. Yoo JI, Shin IS, Jeon JG, Yang YM, Kim JG, Lee DW (2019) The effect of probiotics on halitosis: a systematic review and meta-analysis. Probiotics Antimicrob Proteins 11:150–157. https://doi.org/10.1007/s12602-017-9351-1

    Article  PubMed  Google Scholar 

  16. Olsen I (2015) The periodontal-systemic connection seen from a microbiological standpoint. Acta Odontol Scand 73:563–568. https://doi.org/10.3109/00016357.2015.1007480

    Article  CAS  PubMed  Google Scholar 

  17. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, Huttenhower C, Izard J (2012) Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 13:R42. https://doi.org/10.1186/gb-2012-13-6-r42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sato K, Takahashi N, Kato T, Matsuda Y, Yokoji M, Yamada M, Nakajima T, Kondo N, Endo N, Yamamoto R, Noiri Y, Ohno H, Yamazaki K (2017) Aggravation of collagen-induced arthritis by orally administered Porphyromonas gingivalis through modulation of the gut microbiota and gut immune system. Sci Rep 7:6955. https://doi.org/10.1038/s41598-017-07196-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Olsen I, Yamazaki K (2019) Can oral bacteria affect the microbiome of the gut? J Oral Microbiol 11:1586422. https://doi.org/10.1080/20002297.2019.1586422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. de Souza CB, Roeselers G, Troost F et al (2014) Prebiotic effects of cassava bagasse in TNO’s in vitro model of the colon in lean versus obese microbiota. J Funct Foods 11:210–220. https://doi.org/10.1016/j.jff.2014.09.019

    Article  CAS  Google Scholar 

  21. Arshad NH, Zaman SA, Rawi MH, Sarbini SR (2018) Resistant starch evaluation and in vitro fermentation of lemantak (native sago starch), for prebiotic assessment. Int Food Res J 25:951–957

    CAS  Google Scholar 

  22. Shoaib M, Shehzad A, Omar M, Rakha A, Raza H, Sharif HR, Shakeel A, Ansari A, Niazi S (2016) Inulin: properties, health benefits and food applications. Carbohydr Polym 147:444–454. https://doi.org/10.1016/j.carbpol.2016.04.020

    Article  CAS  PubMed  Google Scholar 

  23. Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777–780. https://doi.org/10.1128/aem.43.4.777-780.1982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Congdon RW, Muth GW, Splittgerber AG (1993) The binding interaction of coomassie blue with proteins. Anal Biochem 213:407–413. https://doi.org/10.1006/abio.1993.1439

    Article  CAS  PubMed  Google Scholar 

  25. Quintelas C, Ferreira EC, Lopes JA, Sousa C (2018) An overview of the evolution of infrared spectroscopy applied to bacterial typing. Biotechnol J 13:1700449. https://doi.org/10.1002/biot.201700449

    Article  CAS  Google Scholar 

  26. Garip S, Bozoglu F, Severcan F (2007) Differentiation of mesophilic and thermophilic bacteria with Fourier transform infrared spectroscopy. Appl Spectrosc 61:186–192. https://doi.org/10.1366/000370207779947486

    Article  CAS  PubMed  Google Scholar 

  27. Lasch P, Naumann D (2015) Infrared spectroscopy in microbiology. In: Meyers RA (ed) Encyclopedia of analytical chemistry, 3rd edn. Wiley, New York, pp 1–32

    Google Scholar 

  28. Movasaghi Z, Rehman S, ur Rehman DI (2008) Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl Spectrosc Rev 43:134–179. https://doi.org/10.1080/05704920701829043

  29. Kardas M, Gozen AG, Severcan F (2014) FTIR spectroscopy offers hints towards widespread molecular changes in cobalt-acclimated freshwater bacteria. Aquat Toxicol 155:15–23. https://doi.org/10.1016/j.aquatox.2014.05.027

    Article  CAS  PubMed  Google Scholar 

  30. Gurbanov R, Simsek Ozek N, Gozen AG, Severcan F (2015) Quick discrimination of heavy metal resistant bacterial populations using infrared spectroscopy coupled with chemometrics. Anal Chem 87:9653–9661. https://doi.org/10.1021/acs.analchem.5b01659

    Article  CAS  PubMed  Google Scholar 

  31. Naumann D, Helm D, Schultz C (1994) Characterization and identification of micro-organisms by FT-IR spectroscopy and FT-IR microscopy. In: Priest F, Ramos-Cormenzana A, Tindall BJ (eds) Bacterial diversity and systematics, 1st edn. Springer, Boston, pp 67–85

    Chapter  Google Scholar 

  32. Gurbanov R, Simsek Ozek N, Tunçer S et al (2018) Aspects of silver tolerance in bacteria: infrared spectral changes and epigenetic clues. J Biophotonics 11:e201700252. https://doi.org/10.1002/jbio.201700252

    Article  CAS  PubMed  Google Scholar 

  33. Slomka V, Herrero ER, Boon N, Bernaerts K, Trivedi HM, Daep C, Quirynen M, Teughels W (2018) Oral prebiotics and the influence of environmental conditions in vitro. J Periodontol 89:708–717. https://doi.org/10.1002/JPER.17-0437

    Article  CAS  PubMed  Google Scholar 

  34. Slomka V, Hernandez-Sanabria E, Herrero ER, Zaidel L, Bernaerts K, Boon N, Quirynen M, Teughels W (2017) Nutritional stimulation of commensal oral bacteria suppresses pathogens: the prebiotic concept. J Clin Periodontol 44:344–352. https://doi.org/10.1111/jcpe.12700

    Article  CAS  PubMed  Google Scholar 

  35. Behera SS, Ray RC, Zdolec N (2018) Lactobacillus plantarum with functional properties: an approach to increase safety and shelf-life of fermented foods. Biomed Res Int 2018:9361614–9361618. https://doi.org/10.1155/2018/9361614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. van Teeseling MCF, de Pedro MA, Cava F (2017) Determinants of bacterial morphology: from fundamentals to possibilities for antimicrobial targeting. Front Microbiol 8:1264. https://doi.org/10.3389/fmicb.2017.01264

    Article  PubMed  PubMed Central  Google Scholar 

  37. Lin T-Y, Santos TMA, Kontur WS, Donohue TJ, Weibel DB (2017) A cardiolipin-deficient mutant of Rhodobacter sphaeroides has an altered cell shape and is impaired in biofilm formation. Biophys J 197:3446–3455. https://doi.org/10.1128/JB.00420-15

    Article  CAS  Google Scholar 

  38. Cui LH, Yan CG, Li HS, Kim WS, Hong L, Kang SK, Choi YJ, Cho CS (2018) A new method of producing a natural antibacterial peptide by encapsulated probiotics internalized with inulin nanoparticles as prebiotics. J Microbiol Biotechnol 28:510–519. https://doi.org/10.4014/jmb.1712.12008

    Article  CAS  PubMed  Google Scholar 

  39. Hong L, Kim WS, Lee SM, Kang SK, Choi YJ, Cho CS (2019) Pullulan nanoparticles as prebiotics enhance the antibacterial properties of Lactobacillus plantarum through the induction of mild stress in probiotics. Front Microbiol 10:142. https://doi.org/10.3389/fmicb.2019.00142

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sah BNP, Vasiljevic T, McKechnie S, Donkor ON (2016) Antibacterial and antiproliferative peptides in synbiotic yogurt-release and stability during refrigerated storage. J Dairy Sci 99:4233–4242. https://doi.org/10.3168/jds.2015-10499

    Article  CAS  PubMed  Google Scholar 

  41. Hassan M, Kjos M, Nes IF, Diep DB, Lotfipour F (2012) Natural antimicrobial peptides from bacteria: characteristics and potential applications to fight against antibiotic resistance. J Appl Microbiol 113:723–736. https://doi.org/10.1111/j.1365-2672.2012.05338.x

    Article  CAS  PubMed  Google Scholar 

  42. Omardien S, Brul S, Zaat SAJ (2016) Antimicrobial activity of cationic antimicrobial peptides against gram-positives: current progress made in understanding the mode of action and the response of bacteria. Front Cell Dev Biol 4:111. https://doi.org/10.3389/fcell.2016.00111

    Article  PubMed  PubMed Central  Google Scholar 

  43. Hols P, Ledesma-García L, Gabant P, Mignolet J (2019) Mobilization of microbiota commensals and their bacteriocins for therapeutics. Trends Microbiol 27:690–702. https://doi.org/10.1016/j.tim.2019.03.007

    Article  CAS  PubMed  Google Scholar 

  44. Kuppusamy R, Willcox M, Black DSC, Kumar N (2019) Short cationic peptidomimetic antimicrobials. Antibiotics 8:44. https://doi.org/10.3390/antibiotics8020044

    Article  CAS  PubMed Central  Google Scholar 

  45. Dept of Pathology & Microbiology; University of Nebraska Medical Center (2020) The Antimicrobial Peptide Database (APD). http://aps.unmc.edu/AP/statistic/statistic_structure.php. Accessed 18 Jan 2020

  46. Falla TJ, Karunaratne DN, Hancock REW (1996) Mode of action of the antimicrobial peptide indolicidin. J Biol Chem 271:19298–19303. https://doi.org/10.1074/jbc.271.32.19298

    Article  CAS  PubMed  Google Scholar 

  47. Hwang PM, Vogel HJ (1998) Structure-function relationships of antimicrobial peptides. Biochem Cell Biol 76:235–246. https://doi.org/10.1139/o98-026

    Article  CAS  PubMed  Google Scholar 

  48. Monie TP (2017) The innate immune system: a compositional and functional perspective. United Kingdom, A snapshot of the innate immune system

  49. Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LMT (2018) Functions and emerging applications of bacteriocins. Curr Opin Biotechnol 49:23–28. https://doi.org/10.1016/j.copbio.2017.07.011

    Article  CAS  PubMed  Google Scholar 

  50. Wood BR (2016) The importance of hydration and DNA conformation in interpreting infrared spectra of cells and tissues. Chem Soc Rev 45:1980–1998. https://doi.org/10.1039/c5cs00511f

    Article  CAS  PubMed  Google Scholar 

  51. Kopaczynska M, Schulz A, Fraczkowska K, Kraszewski S, Podbielska H, Fuhrhop JH (2016) Selective condensation of DNA by aminoglycoside antibiotics. Eur Biophys J 45:287–299. https://doi.org/10.1007/s00249-015-1095-9

    Article  CAS  PubMed  Google Scholar 

  52. Temiz NA, Donohue DE, Bacolla A, Luke BT, Collins JR (2012) The role of methylation in the intrinsic dynamics of B- and Z-DNA. PLoS One 7:e35558. https://doi.org/10.1371/journal.pone.0035558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gurbanov R, Tunçer S, Mingu S, Severcan F, Gozen AG (2019) Methylation, sugar puckering and Z-form status of DNA from a heavy metal-acclimated freshwater Gordonia sp. J Photochem Photobiol B Biol 198:111580. https://doi.org/10.1016/j.jphotobiol.2019.111580

    Article  CAS  Google Scholar 

  54. Lammers KM, Brigidi P, Vitali B, Gionchetti P, Rizzello F, Caramelli E, Matteuzzi D, Campieri M (2003) Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 38:165–172. https://doi.org/10.1016/S0928-8244(03)00144-5

    Article  CAS  PubMed  Google Scholar 

  55. Krieg AM (2002) CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20:709–760. https://doi.org/10.1146/annurev.immunol.20.100301.064842

    Article  CAS  PubMed  Google Scholar 

  56. Wang LH, Zeng XA, Wang MS, Brennan CS, Gong D (2018) Modification of membrane properties and fatty acids biosynthesis-related genes in Escherichia coli and Staphylococcus aureus: implications for the antibacterial mechanism of naringenin. Biochim Biophys Acta Biomembr 1860:481–490. https://doi.org/10.1016/j.bbamem.2017.11.007

    Article  CAS  PubMed  Google Scholar 

  57. Zhu B, Xia X, Xia N, Zhang S, Guo X (2014) Modification of fatty acids in membranes of bacteria: implication for an adaptive mechanism to the toxicity of carbon nanotubes. Environ Sci Technol 48:4086–4095. https://doi.org/10.1021/es404359v

    Article  CAS  PubMed  Google Scholar 

  58. Boudjemaa R, Cabriel C, Dubois-Brissonnet F, Bourg N, Dupuis G, Gruss A, Lévêque-Fort S, Briandet R, Fontaine-Aupart MP, Steenkeste K (2018) Impact of bacterial membrane fatty acid composition on the failure of daptomycin to kill Staphylococcus aureus. Antimicrob Agents Chemother 62:e00023–e00018. https://doi.org/10.1128/AAC.00023-18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Poole J, Day CJ, von Itzstein M, Paton JC, Jennings MP (2018) Glycointeractions in bacterial pathogenesis. Nat Rev Microbiol 16:440–452. https://doi.org/10.1038/s41579-018-0007-2

    Article  CAS  PubMed  Google Scholar 

  60. Zannini E, Waters DM, Coffey A, Arendt EK (2016) Production, properties, and industrial food application of lactic acid bacteria-derived exopolysaccharides. Appl Microbiol Biotechnol 100:1121–1135. https://doi.org/10.1007/s00253-015-7172-2

    Article  CAS  PubMed  Google Scholar 

  61. Castro-Bravo N, Wells JM, Margolles A, Ruas-Madiedo P (2018) Interactions of surface exopolysaccharides from Bifidobacterium and Lactobacillus within the intestinal environment. Front Microbiol 2018:2426. https://doi.org/10.3389/fmicb.2018.02426

    Article  Google Scholar 

  62. Kim Y, Oh S, Kim SH (2009) Released exopolysaccharide (r-EPS) produced from probiotic bacteria reduce biofilm formation of enterohemorrhagic Escherichia coli O157:H7. Biochem Biophys Res Commun 379:324–329. https://doi.org/10.1016/j.bbrc.2008.12.053

    Article  CAS  PubMed  Google Scholar 

  63. Rendueles O, Kaplan JB, Ghigo JM (2013) Antibiofilm polysaccharides. Environ Microbiol 15:334–346. https://doi.org/10.1111/j.1462-2920.2012.02810.x

    Article  CAS  PubMed  Google Scholar 

  64. Wang M, Chen Y, Wang Y, Li Y, Zheng H, Ma F, Ma CW, Zhang X, Lu B, Xie Z, Liao Q (2018) The effect of probiotics and polysaccharides on the gut microbiota composition and function of weaned rats. Food Funct 9:1864–1877. https://doi.org/10.1039/c7fo01507k

    Article  CAS  PubMed  Google Scholar 

  65. Sánchez B, Delgado S, Blanco-Míguez A, Lourenço A, Gueimonde M, Margolles A (2017) Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res 61:1600240. https://doi.org/10.1002/mnfr.201600240

    Article  CAS  Google Scholar 

  66. Živković M, Miljković MS, Ruas-Madiedo P, et al (2016) EPS-SJ exopolisaccharide produced by the strain Lactobacillus paracasei subsp. paracasei BGSJ2-8 is involved in adhesion to epithelial intestinal cells and decrease on E. coli association to Caco-2 cells. Front Microbiol 7:286. https://doi.org/10.3389/fmicb.2016.00286

  67. Goh YJ, Klaenhammer TR (2013) A functional glycogen biosynthesis pathway in Lactobacillus acidophilus: expression and analysis of the glg operon. Mol Microbiol 89:1187–1200. https://doi.org/10.1111/mmi.12338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kaulpiboon J, Rudeekulthamrong P, Watanasatitarpa S, Ito K, Pongsawasdi P (2015) Synthesis of long-chain isomaltooligosaccharides from tapioca starch and an in vitro investigation of their prebiotic properties. J Mol Catal B Enzym 120:127–135. https://doi.org/10.1016/j.molcatb.2015.07.004

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rafig Gurbanov.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

ESM 1

(DOCX 5345 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gurbanov, R., Karadağ, H., Karaçam, S. et al. Tapioca Starch Modulates Cellular Events in Oral Probiotic Streptococcus salivarius Strains. Probiotics & Antimicro. Prot. 13, 195–207 (2021). https://doi.org/10.1007/s12602-020-09678-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-020-09678-z

Keywords

Navigation