Advertisement

Low-Dose Electron-Beam Irradiation for the Improvement of Biofilm Formation by Probiotic Lactobacilli

  • Astghik Z. PepoyanEmail author
  • Anahit M. Manvelyan
  • Marine H. Balayan
  • Samvel Galstyan
  • Vardan V. Tsaturyan
  • Bagrat Grigoryan
  • Michael L. Chikindas
Article
  • 15 Downloads

Abstract

The effects of 50–150 gray electron-beam irradiation on the biofilm-formation ability and cell surface hydrophobicity of the commercial strain, Lactobacillus acidophilus DDS®-1, from Lacto-G (a marketed synbiotic formulation) and the putative probiotic, L. rhamnosus Vahe, were evaluated. No significant changes in cell surface hydrophobicity were found after irradiation, while increases in biofilm-formation abilities were documented for both investigated microorganisms 0.22 ± 0.03 vs. 0.149 ± 0.02 (L. rhamnosus Vahe, 150 Gy) and 0.218 ± 0.021 vs. 0.17 ± 0.012 (L. acidophilus DDS®-1, 150 Gy). Given this, the use of electron-beam irradiation (50–100 Gy) for the treatment of L. rhamnosus Vahe and L. acidophilus DDS®-1 cells may be considered in product sterilization, quality improvement, and packaging practices.

Keywords

Lactobacillus Hydrophobicity Biofilm Probiotic 

Notes

Funding

This study was funded by a grant from the International Science and Technology Center (A-2134), and the “CANDLE” Synchrotron Research Institute foundation (17A-1F010). MC was supported in part by the Ministry of Science and Higher Education of the Russian Federation (project 19.6015.2017/8.9).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

References

  1. 1.
    Lacroix M, Follett P (2015) Combination irradiation treatments for food safety and phytosanitary uses. Stewart Postharvest Rev 11:1–10.  https://doi.org/10.2212/spr.2015.3.4 Google Scholar
  2. 2.
    Pillai S (2016) Introduction to electron-beam food irradiation. Chem Eng Prog 112:36–44 https://www.aiche.org/resources/publications/cep/2016/november/introduction-electron-beam-food-irradiation Google Scholar
  3. 3.
    Odueke B, Farag K, Baines R (2016) Irradiation applications in dairy products: a review. Food Bioprocess Technol 9:751–767.  https://doi.org/10.1007/s11947-016-1709-y CrossRefGoogle Scholar
  4. 4.
    Hill C, Guarner F, Reid G, Gibson G, Merenstein D, Pot B (2014) Expert consensus document: the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514.  https://doi.org/10.1038/nrgastro.2014.66 CrossRefGoogle Scholar
  5. 5.
    Champagne CP, Gomes da Cruz A, Daga M (2018) Strategies to improve the functionality of probiotics in supplements and foods. Curr Opin Food Sci 22:160–166.  https://doi.org/10.1016/j.cofs.2018.04.008 CrossRefGoogle Scholar
  6. 6.
    Thomas LV (2016) Probiotics – the journey continues. Int J Dairy Technol 69:469–480.  https://doi.org/10.1111/1471-0307.12354 CrossRefGoogle Scholar
  7. 7.
    Guimarães J, Balthazar C, Scudino H, Pimentel T, Cruz A (2019) High-intensity ultrasound: a novel technology for the development of probiotic and prebiotic dairy products. Ultrason Sonochem 57:12–21.  https://doi.org/10.1016/j.ultsonch.2019.05.004 CrossRefGoogle Scholar
  8. 8.
    Muramalla T, Aryana K (2011) Some low homogenization pressures improve certain probiotic characteristics of yogurt culture bacteria and Lactobacillus acidophilus LA-K. J Dairy Sci 94:3725–3738.  https://doi.org/10.3168/jds.2010-3737 CrossRefGoogle Scholar
  9. 9.
    Hasani S, Sari A, Heshmati A, Karami M (2017) Physicochemical and sensory attributes assessment of functional low-fat yogurt produced by incorporation of barley bran and Lactobacillus acidophilus. Food Sci Nutr 5:875–880.  https://doi.org/10.1002/fsn3.470 CrossRefGoogle Scholar
  10. 10.
  11. 11.
    Dong J, Liu B, Jiang T, Liu Y, Chen L (2017) The biofilm hypothesis: the formation mechanism of Tibetan kefir grains. Int J Dairy Technol 71:44–50.  https://doi.org/10.1111/1471-0307.12473 CrossRefGoogle Scholar
  12. 12.
    Kankaanpaa P, Yang B, Kallio H, Isolauri E, Salminen S (2004) Effects of polyunsaturated fatty acids in growth medium on lipid composition and on physicochemical surface properties of lactobacilli. Appl Environ Microbiol 70:129–136.  https://doi.org/10.1128/AEM.70.1.129-136.2004 CrossRefGoogle Scholar
  13. 13.
    Pepoyan A, Balayan M, Manvelyan A, Pepoyan S (2018) Cell surface hydrophobicity and biofilm formation potential of gut commensal Escherichia coli and lactobacilli from Mazekh and Balbas sheep. Bulletin of State Agrarian University of Armenia 1:51–54 UDC: 631.95(479.25)Google Scholar
  14. 14.
    Vadillo-Rodríguez V, Busscher H, Norde W (2004) Dynamic cell surface hydrophobicity of Lactobacillus strains with and without surface layer proteins. J Bacteriol 186:6647–6650.  https://doi.org/10.1128/JB.186.19.6647-6650.2004 CrossRefGoogle Scholar
  15. 15.
    Lebeer S, Verhoeven TL, Perea M, Velez VJ, Keersmaecker SC (2007) Impact of environmental and genetic factors on biofilms formation by the probiotic strain Lactobacillus rhamnosus GG. Appl Environ Microbiol 73:6768–6775.  https://doi.org/10.1128/AEM.01393-07 CrossRefGoogle Scholar
  16. 16.
    Kubota H, Senda S, Nomura N, Tokuda H, Uchiyama H (2008) Biofilm formation by lactic acid bacteria and resistance to environmental stress. J Biosci Bioeng 106:381–386.  https://doi.org/10.1263/jbb.106.381 CrossRefGoogle Scholar
  17. 17.
    Vemuri R, Shinde T, Shastri MD, Perera AP, Tristram S, Martoni CJ, Gundamaraju R, Ahuja KDK, Ball M, Eri R (2018) A human origin strain Lactobacillus acidophilus DDS-1 exhibits superior in vitro probiotic efficacy in comparison to plant or dairy origin probiotics. Int J Med Sci 15:840–848.  https://doi.org/10.7150/ijms.25004 CrossRefGoogle Scholar
  18. 18.
    Vemuri R, Shinde T, Gundamaraju R, Gondalia SV, Karpe AV, Beale DJ, Martoni CJ, Eri R (2018) Lactobacillus acidophilus DDS-1 modulates the gut microbiota and improves metabolic profiles in aging mice. Nutrients 10(9):1255.  https://doi.org/10.3390/nu10091255 CrossRefGoogle Scholar
  19. 19.
    Pakdaman MN, Udani JK, Molina JP, Shahani M (2016) The effects of the DDS-1 strain of lactobacillus on symptomatic relief for lactose intolerance: a randomized, double-blind, placebo-controlled, crossover clinical trial. Nutr J 15:56.  https://doi.org/10.1186/s12937-016-0172-y CrossRefGoogle Scholar
  20. 20.
    Pepoyan A, Balayan M, Manvelyan A, Galstyan L, Pepoyan S, Petrosyan S, Tsaturyan V, Kamiya S, Torok T, Chikindas M (2018) Probiotic Lactobacillus acidophilus strain INMIA 9602 Er 317/402 administration reduces the numbers of Candida albicans and abundance of enterobacteria in the gut microbiota of familial Mediterranean fever patients. Front Immunol 9:1426.  https://doi.org/10.3389/fimmu.2018.01426 CrossRefGoogle Scholar
  21. 21.
    Pepoyan AZ, Balayan M, Manvelyan A, Pepoyan S, Malkhasyan L, Bezhanyan T, Paronikyan R, Malakyan M, Bajinyan S, Tsaturyan V, Kamiya S, Chikindas M (2018) Radioprotective effects of lactobacilli with antagonistic activities against human pathogens. Biophys J 114(3):665a.  https://doi.org/10.1016/j.bpj.2017.11.3586 CrossRefGoogle Scholar
  22. 22.
    Pepoyan A, Balayan M, Malkasyan L, Manvelyan A, Bezhanyan T, Paronikyan R, Tsaturyan V, Tatikyan S, Kamiya S, Chikindas M (2018) Effects of probiotic Lactobacillus acidophilus strain INMIA 9602 Er 317/402 and putative probiotic lactobacilli on DNA damages in small intestine of Wistar rats in vivo. Probiotics Antimicrob Proteins.  https://doi.org/10.1007/s12602-018-9491-y. Epub ahead of print
  23. 23.
    Tsakanov VM, Aroutiounian RM, Amatuni GA, Aloyan LR, Aslanyan LG, Avagyan VS, Babayan NS, Buniatyan VV, Dalyan YB, Davtyan HD, Derdzyan MV, Grigoryan BA, Grigoryan NE, Hakobyan LS, Haroutyunian SG, Harutiunyan VV, Hovhannesyan KL, Khachatryan VG, Martirosyan NW, Melikyan GS, Petrosyan AG, Petrosyan VH, Sahakyan AA, Sahakyan VV, Sargsyan AA, Simonyan AS, Tatikyan SS, Tsakanova GV, Tsovyan E, Vardanyan AS, Vardanyan VV, Yeremyan AS, Yeritsyan HN, Zanyan GS (2016) AREAL low energy electron beam applications in life and materials sciences. Nucl Instrum Methods Phys Res A 829:248–253.  https://doi.org/10.1016/j.nima.2016.02.028i CrossRefGoogle Scholar
  24. 24.
    Kos B, Šušković J, Vuković S, Šimpraga M, Frece J, Matošić S (2003) Adhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M29. J Appl Microbiol 94:981–987.  https://doi.org/10.1046/j.1365-2672.2003.01915.x CrossRefGoogle Scholar
  25. 25.
    Chew S, Cheah Y, Sandai H, Then L (2015) In vitro modulation of probiotic bacteria on the biofilm of Candida glabrata. Anaerobe 34:132–138.  https://doi.org/10.1016/j.anaerobe.2015.05.009 CrossRefGoogle Scholar
  26. 26.
    Tahmourespour A, Kermanshahi R (2011) The effect of a probiotic strain Lactobacillus acidophilus on the plaque formation of oral streptococci. Bosn J Basic Med Sci 11:37–40.  https://doi.org/10.17305/bjbms.2011.2621 CrossRefGoogle Scholar
  27. 27.
    Grajek K, Sip A, Foksowicz-Flaczyk J, Dobrowolska A, Wita A (2016) Adhesive and hydrophobic properties of the selected LAB isolated from gastrointestinal tract of farming animals. Acta Biochim Pol 63:311–314.  https://doi.org/10.18388/abp.2015_1128 CrossRefGoogle Scholar
  28. 28.
    Giaouris E, Chapot-Chartier M, Briandet R (2009) Surface physicochemical analysis of natural Lactococcus lactis strains reveals the existence of hydrophobic and low charged strains with altered adhesive properties. Int J Food Microbiol 131:2–9.  https://doi.org/10.1016/j.ijfoodmicro.2008.09.006 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Food Safety and BiotechnologyArmenian National Agrarian UniversityYerevanArmenia
  2. 2.International Association for Human and Animals Health ImprovementYerevanArmenia
  3. 3.Yerevan State Medical UniversityYerevanArmenia
  4. 4.CANDLE Synchrotron Research InstituteYerevanArmenia
  5. 5.Health Promoting Naturals LaboratoryRutgers State UniversityNew BrunswickUSA
  6. 6.Academy of Biology and BiotechnologySouthern Federal UniversityRostov-on-DonRussia

Personalised recommendations