Skip to main content

Immunobiosis and probiosis: antimicrobial activity of lactic acid bacteria with a focus on their antiviral and antifungal properties

A Correction to this article was published on 17 October 2018

This article has been updated

Abstract

Lactic acid bacteria (LAB), a heterogeneous group of bacteria that produce lactic acid as the main product of carbohydrate degradation, play an important role in the production and protection of fermented foods. Moreover, beside the technological use of these microorganisms added to control and steer food fermentations, their beneficial healthy properties are largely overt. Thus, numerous LAB strains have obtained the probiotic status, which entails the ability to maintain and promote a good health of consumers. In particular, increasing consideration is being focused on probiotic microorganisms that can improve the human immune response against dangerous viral and fungal enemies. For such beneficial microbes, the term “immunobiotics” has been coined. Together with an indirect host-mediated adverse effect against undesirable microorganisms, also a direct antagonistic activity of several LAB strains has been largely demonstrated. The purpose of this review is to provide a fullest possible overview of the antiviral and antifungal activities ascribed to probiotic LAB. The interest in this research field is substantiated by a large number of studies exploring the potential application of these beneficial microorganisms both as biopreservatives and immune-enhancers, aiming to reduce and/or eliminate the use of chemical agents to prevent the development of pathogenic, infectious, and/or degrading causes.

This is a preview of subscription content, access via your institution.

Fig. 1

Change history

  • 17 October 2018

    There is an error in the original publication of this paper. The incorrect author name was captured as "Djamel Dridier" instead of "Djamel Drider". The original article has been corrected.

References

  1. Agarwal KN, Bhasin SK (2002) Feasibility studies to control acute diarrhea in children by feeding fermented milk preparations Actimel and Indian Dahi. Eur J Clin Nutr 56:S56–S59

    PubMed  Google Scholar 

  2. Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D (2014) Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob Proteins 6:177–185

    CAS  PubMed  Google Scholar 

  3. Al Kassaa I, Hober D, Hamze M, Caloone D, Dewilde A, Chihib NE, Drider D (2015) Vaginal Lactobacillus gasseri CMUL57 can inhibit herpes simplex type 2 but not Coxsackievirus B4E2. Arch Microbiol 197:657–664

    CAS  PubMed  Google Scholar 

  4. Al-Tawaha R, Meng C (2018) Potential benefits of Lactobacillus plantarum as probiotic and its advantages in human health and industrial applications: a review. Adv Environ Biol 12:16–27

    Google Scholar 

  5. Ang LYE, Too HKI, Tan EL, Chow TKV, Shek PCL, Tham E, Alonso S (2016) Antiviral activity of Lactobacillus reuteri Protectis against Coxsackievirus A and Enterovirus 71 infection in human skeletal muscle and colon cell lines. Virol J 13:111–123

    PubMed  PubMed Central  Google Scholar 

  6. Arena MP, Capozzi V, Spano G, Fiocco D (2017) The potential of lactic acid bacteria to colonize biotic and abiotic surfaces and the investigation of their interactions and mechanisms. Appl Microbiol Biotechnol 101:2641–2657

    CAS  PubMed  Google Scholar 

  7. Arena MP, Elmastour F, Sane F, Drider D, Fiocco D, Spano G, Hober D (2018) Inhibition of coxsackievirus B4 by Lactobacillus plantarum. Microbiol Res 210:59–64

    CAS  PubMed  Google Scholar 

  8. Arena MP, Silvain A, Normanno G, Grieco F, Drider D, Spano G, Fiocco D (2016) Use of Lactobacillus plantarum strains as a bio-control strategy against food-borne pathogenic microorganisms. Front Microbiol 7:464–474

    PubMed  PubMed Central  Google Scholar 

  9. Arena MP, Russo P, Capozzi V, López P, Fiocco D, Spano G (2014) Probiotic abilities of riboflavin-overproducing Lactobacillus strains: a novel promising application of probiotics. Appl Microbiol Biotechnol 98(17):7569–7581

    CAS  PubMed  Google Scholar 

  10. Arqués JL, Rodríguez E, Langa S, Landete JM, Medina M (2015) Antimicrobial activity of lactic acid bacteria in dairy products and gut: effect on pathogens. Biomed Res Int 2015:1–10

    Google Scholar 

  11. Aunsbjerg SD, Honoré AH, Marcussen J, Ebrahimi P, Vogensen FK, Benfeldt C, Skov T, Knøchel S (2015) Contribution of volatiles to the antifungal effect of Lactobacillus paracasei in defined medium and yogurt. Int J Food Microbiol 194:46–53

    CAS  PubMed  Google Scholar 

  12. Axel C, Röcker B, Brosnan B, Zannini E, Furey A, Coffey A, Arendt EK (2015) Application of Lactobacillus amylovorus DSM19280 in gluten-free sourdough bread to improve the microbial shelf life. Food Microbiol 47:36–44

    CAS  PubMed  Google Scholar 

  13. Axelsson L (2004) Lactic acid bacteria: classification and physiology. In: Salminen S, von Wright A, Ouwehand A (eds) Lactic acid bacteria. Marcel Dekker, New York, pp 1–66

    Google Scholar 

  14. Bermudez-Brito M, Plaza-Dıaz J, Munoz-Quezada S, Gomez-Llorente C, Gil A (2012) Probiotic mechanisms of action. Ann Nutr Metab 61:160–174

    CAS  PubMed  Google Scholar 

  15. Boge T, Remigy M, Vaudaine S, Tanguy J, Bourdet-Sicard R, van der Werf S (2009) A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine 27:5677–5684

    CAS  PubMed  Google Scholar 

  16. Bonnardel J, Da Silva C, Henri S, Tamoutounour S, Chasson L, Montañana-Sanchis F, Gorvel JP, Lelouard H (2015) Innate and adaptive immune functions of Peyer’s patch monocyte-derived cells. Cell Rep 11: 770–784. doi:https://doi.org/10.1016/j.celrep.2015.03.067

    CAS  PubMed  Google Scholar 

  17. Botić T, Danø T, Weingartl H, Cencič A (2007) A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol 115:227–234

    PubMed  Google Scholar 

  18. Bravo D, Rodríguez E, Medina M (2009) Nisin and lacticin coproduction by Lactococcus lactis strains isolated from raw ewes’ milk. J Dairy Sci 92:4805–4811

    CAS  PubMed  Google Scholar 

  19. Cavera VL, Arthur TD, Kashtanov D, Chikindas ML (2015) Bacteriocins and their position in the next wave of conventional antibiotics. Int J Antimicrob Agents 46:494–501

    CAS  PubMed  Google Scholar 

  20. Cha MK, Lee DK, An HM, Lee SW, Shin SH, Kwon JH, Kim KJ, Ha NJ (2012) Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med 10:72–77

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Champagne CP, Fustier P (2007) Microencapsulation for the improved delivery of bioactive compounds into foods. Curr Opin Biotechnol 18:184–190

    CAS  PubMed  Google Scholar 

  22. Chen H, Hoover DG (2003) Bacteriocins and their food applications. Compr Rev Food Sci Food Saf 2:82–100

    CAS  Google Scholar 

  23. Cheong EYL, Sandhu A, Jayabalan J, Kieu Le TT, Nhiep NT, My Ho HT, Zwielehner J, Bansal N, Turner MS (2014) Isolation of lactic acid bacteria with antifungal activity against the common cheese spoilage mould Penicillium commune and their potential as biopreservatives in cheese. Food Control 46:91–97

    CAS  Google Scholar 

  24. Chiba E, Tomosada Y, Guadalupe MVP, Salva S (2013) Immunobiotic Lactobacillus rhamnosus improves resistance of infant mice against respiratory syncytial virus infection. Int Immunopharmacol 17:373–382

    CAS  PubMed  Google Scholar 

  25. Collins FW, O’Connor PM, O’Sullivan O, Gómez-Sala B, Rea MC, Hill C, Ross RP (2017) Bacteriocin gene-trait matching across the complete Lactobacillus pan-genome. Sci Rep 7:3481–3494

    PubMed  PubMed Central  Google Scholar 

  26. Conti C, Malacrino C, Mastromarino P (2009) Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J Physiol Pharmacol 6:19–26

    Google Scholar 

  27. Cortés-Zavaleta O, López-Malo A, Hernández-Mendoza A, García HS (2014) Antifungal activity of lactobacilli and its relationship with 3-phenyllactic acid production. Int J Food Microbiol 173:30–35

    PubMed  Google Scholar 

  28. Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788

    CAS  PubMed  Google Scholar 

  29. Crowley S, Mahony J, van Sinderen D (2012) Broad-spectrum antifungal-producing lactic acid bacteria and their application in fruit models. Folia Microbiol 58:291–299

    Google Scholar 

  30. Crowley S, Mahony J, van Sinderen D (2013) Current perspectives on antifungal lactic acid bacteria as natural bio-preservatives. Trends Food Sci Technol 33:93–109

    CAS  Google Scholar 

  31. Da Silva FFP, Biscola V, LeBlanc JG, de Melo Franco BDG (2016) Effect of indigenous lactic acid bacteria isolated from goat milk and cheeses on folate and riboflavin content of fermented goat milk. LWT-Food Sci Technol 71:155–161

    Google Scholar 

  32. de Moreno de LeBlanc A, Levit R, de Giori GS, LeBlanc JG (2018) Vitamin producing lactic acid bacteria as complementary treatments for intestinal inflammation. Antiinflamm Antiallergy Agents Med Chem 17:50–56

    PubMed  Google Scholar 

  33. Diener M (2016) Roadblock for antigens – take a detour via M cells. Acta Physiol 216:13–14. https://doi.org/10.1111/apha.12595

    CAS  Article  Google Scholar 

  34. Egan K, Field D, Rea MC, Ross RP, Hill C, Cotter PD (2016) Bacteriocins: novel solutions to age old spore-related problems? Front Microbiol 7:461–482. https://doi.org/10.3389/fmicb.2016.00461

    Article  PubMed  PubMed Central  Google Scholar 

  35. Galdeano CM, De Leblanc ADM, Vinderola G, Bonet MB, Perdigon G (2007) Proposed model: mechanisms of immunomodulation induced by probiotic bacteria. Clinical Vaccine Immunol 14:485–492

    CAS  Google Scholar 

  36. Garrity GM, Holt JG (2001) The road map to the manual. In: Bergey’s manual® of systematic bacteriology. Springer, New York, pp 119–166

    Google Scholar 

  37. Garsa AK, Kumariya R, Kumar A, Lather P, Kapila S, Sood S (2014) Industrial cheese whey utilization for enhanced production of purified pediocin PA-1. LWT Food Sci Technol 59:656–665. https://doi.org/10.1016/j.lwt.2014.07.008

    CAS  Article  Google Scholar 

  38. Garvey GS, McCormick SP, Rayment I (2008) Structural and functional characterization of the TRI101 trichothecene 3-O-acetyltransferase from Fusarium sporotrichioides and Fusarium graminearum: kinetic insights to combating Fusarium head blight. J Biol Chem 283:1660–1669

    CAS  PubMed  Google Scholar 

  39. Favaro L, Penna ALB, Todorov SD (2015) Bacteriocinogenic LAB from cheeses–application in biopreservation? Trends Food Sci Technol 41:37–48. https://doi.org/10.1016/j.tifs.2014.09.001

    CAS  Article  Google Scholar 

  40. FAO/WHO (2001) Health and nutrition properties of probiotics in food including powder milk with live lactic acid bacteria. Retrieved from http://www.who.int/foodsafety/ publications/fs_management/probiotics/en/index.html

  41. Franz CM, Holzapfel WH (2011) The importance of understanding the stress physiology of lactic acid bacteria. In: Stress responses of lactic acid bacteria. Springer, Boston, MA, pp 3–20

    Google Scholar 

  42. Hanson L, VandeVusse L, Jermé M, Abad CL, Safdar N (2016) Probiotics for treatment and prevention of urogenital infections in women: a systematic review. J Midwifery Women's health 61:339–355

    Google Scholar 

  43. Héchard Y, Sahl HG (2002) Mode of action of modified and unmodified bacteriocins from Gram-positive bacteria. Biochimie 84:545–557

    PubMed  Google Scholar 

  44. Hathout AS, Ali SE (2014) Biological detoxification of mycotoxins: a review. Annals Microbiol 64(3):905–919

    CAS  Google Scholar 

  45. Humaira Q, Sadia S, Ahmed S, Ajaz Rasool S (2006) Coliphage hsa as a model for antiviral studies/spectrum by some indigenous bacteriocin like inhibitory substances (BLIS). Pak J Pharma Sci 19:182–187

    Google Scholar 

  46. Isolauri E (1999) Immune e!Ects of probiotics. In: Hanson LA, Yolken RH, Probiotics, other nutritional factors and intestinal microyora, Vevey/Lippincott-Raven Publishers, Philadelphia, pp 229–241

  47. Jeon SH, Kim NH, Shim MB, Jeon YW, Ahn JH, Lee SH, Hwang IG, Rhee MS (2015) Microbiological diversity and prevalence of spoilage and pathogenic bacteria in commercial fermented alcoholic beverages (beer, fruit wine, refined rice wine, and yakju). J Food Prot 78:812–818

    PubMed  Google Scholar 

  48. Juodeikiene G, Bartkiene E, Cernauskas D, Cizeikiene D, Zadeike D, Lele V, Bartkevics V (2018) Antifungal activity of lactic acid bacteria and their application for Fusarium mycotoxin reduction in malting wheat grains. LWT-Food Sci Technol 89:307–314

    CAS  Google Scholar 

  49. Jyoti B, Suresh AK, Venkatesh K (2003) Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World J Microbiol Biotechnol 19:509–515

    CAS  Google Scholar 

  50. Khania S, Motamedifara M, Golmoghaddam H, Hosseinic HM, Hashemizadeha Z (2012) In vitro study of the effect of a probiotic bacterium Lactobacillus rhamnosus against herpes simplex virus type 1. Braz J Infect Dis 16:129–135

    Google Scholar 

  51. Karlovsky P (1999) Biological detoxification of fungal toxins and its use in plant breeding, feed and food production. Nat Toxins 7:1–23

    CAS  PubMed  Google Scholar 

  52. Kim MJ, Lee DK, Park JE, Park IH, Seo JG, Ha NJ (2014) Antiviral activity of Bifidobacterium adolescentis SPM1605 against coxsackievirus B3. Biotechnol Biotechnol Equip 28:681–688

    PubMed  PubMed Central  Google Scholar 

  53. Kleerebezem M, Kuipers OP, Smid EJ (2017) Editorial: lactic acid bacteria-a continuing journey in science and application. FEMS Microbiol Rev 1. 41(Supp_1):S1-S2. doi: https://doi.org/10.1093/femsre/fux036

    PubMed  Google Scholar 

  54. Kumar P, Chatli MK, Verma AK, Mehta N, Malav OP, Kumar D, Sharma N (2017) Quality, functionality, and shelf life of fermented meat and meat products: a review. Critical Rev Food Sci Nutrition 57:2844–2856

    CAS  Google Scholar 

  55. Laissue JA, Chappuis BB, MuKller C, Reubi JC, Gebbers J-O (1993) The intestinal immune system and its relation to disease. Digestive Dis 11:298–312

    CAS  Google Scholar 

  56. Lanciotti R, Patrignani F, Bagnolini F, Guerzoni ME, Gardini F (2003) Evaluation of diacetyl antimicrobial activity against Escherichia coli, Listeria monocytogenes and Staphylococcus aureus. Food Microbiol 20:537–543

    CAS  Google Scholar 

  57. Lavermicocca P, Valerio F, Evidente A, Lazzaroni S, Corsetti A, Gobbetti M (2000) Purification and characterization of novel antifungal compounds from the sourdough Lactobacillus plantarum strain 21B. Appl Environ Microbiol 66:4084–4090

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Lazarus RP, John J, Shanmugasundaram E, Rajan AK, Thiagarajan S, Giri S, Babji S, Sarkar R, Kaliappan PS, Venugopal S, Praharaj I, Raman U, Paranjpe M, Grassly NC, Parker EPK, Parashar UD, Tate JE, Fleming JA, Steele AD, Muliyil J, Abraham AM, Kang G (2018) The effect of probiotics and zinc supplementation on the immune response to oral rotavirus vaccine: a randomized, factorial design, placebo-controlled study among Indian infants. Vaccine 36:273–279

    CAS  PubMed  Google Scholar 

  59. Li GL, Jiang W, Xia Q, Chen SH, Ge XR, Gui SQ, Xu CJ (2010) HPV E6 downregulation and apoptosis induction of human cervical cancer cells by a novel lipid-soluble extract (PE) from Pinellia pedatisecta Schott in vitro. J Ethnopharmacol 132:56–64

    PubMed  Google Scholar 

  60. Lorca GL, de Valdez GF (2009) Lactobacillus stress responses. In: Lactobacillus molecular biology: from genomics to probiotics, Å Ljungh, T Wadström (Eds.), Caister Academic Press, Norfolk, UK, pp. 115–138

  61. López-Cuellar MDR, Rodríguez-Hernández AI, Chavarría-Hernández N (2016) LAB bacteriocin applications in the last decade. Biotechnol Biotechnol Equipment 30:1039–1050

    Google Scholar 

  62. Maeda N, Nakamura R, Hirose Y, Murosaki S, Yamamoto Y, Kase T, Yoshikai Y (2009) Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. Int Immunopharmacol 9:1122–1125

    CAS  PubMed  Google Scholar 

  63. Malhotra B, Keshwani A, Kharkwal H (2015) Antimicrobial food packaging: potential and pitfalls. Frontiers Microbiol 6:611–619

    Google Scholar 

  64. Mailänder-Sánchez D, Braunsdorf C, Grumaz C, Müller C, Lorenz S, Stevens P, Wagener J, Hebecker B, Hube B, Bracher F, Sohn K, Schaller M (2017) Antifungal defense of probiotic Lactobacillus rhamnosus GG is mediated by blocking adhesion and nutrient depletion. PLoS One 12:e0184438

    PubMed  PubMed Central  Google Scholar 

  65. Majamaa H, Isolauri E, Saxelin M, Vesikari T (1995) Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatric Gastroenterol Nutrtion 20:333–338

    CAS  Google Scholar 

  66. Maragkoudakis PA, Chingwaru W, Gradisnik L, Tsakalidou E, Cencic A (2010) Lactic acid bacteria efficiently protect human and animal intestinal epithelial and immune cells from enteric virus infection. Int J Food Microbiol 141:S91–S97

    PubMed  Google Scholar 

  67. Martin LS, McDougal JS, Loskoski SL (1985) Disinfection and inactivation of the human lymphotropic virus type III/lymphadenopathy- associated virus. J Infect Dis 152:400–403

    CAS  PubMed  Google Scholar 

  68. Martin V, Maldonado A, Fernandez L, Rodriguez JM, Connor RI (2010) Inhibition of human immunodeficiency virus type 1 by lactic acid bacteria from human breastmilk. Breastfeed Med 5:153–158

    PubMed  PubMed Central  Google Scholar 

  69. Mastromarino P, Cacciotti F, Masci A, Mosca L (2011) Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: role of cell wall associated components. Anaerobe 17:334–336

    PubMed  Google Scholar 

  70. McCormick SP (2013) Microbial detoxification of mycotoxins. J Chemical Ecol 39(7):907–918

    CAS  Google Scholar 

  71. Mendonça FHBP, Santos SSFD, Faria IDSD, Gonçalves Silva CR, Jorge AOC, Leão MVP (2012) Effects of probiotic bacteria on Candida presence and IgA anti-Candida in the oral cavity of elderly. Brazilian Dental J 23:534–538

    Google Scholar 

  72. Mieszkin S, Hymery N, Debaets S, Coton E, Le Blay G, Valence F, Mounier J (2017) Action mechanisms involved in the bioprotective effect of Lactobacillus harbinensis K.V9.3.1.Np against Yarrowia lipolytica in fermented milk. Int J Food Microbiol 248:47–55

    CAS  PubMed  Google Scholar 

  73. Mombelli B, Gismondo MR (2000) The use of probiotics in medical practice. Int J Antimicrob Agents 16:531–536

    CAS  PubMed  Google Scholar 

  74. Niku-Paavola ML, Laitila A, Mattila-Sandholm T, Haikara A (1999) New types of antimicrobial compounds produced by Lactobacillus plantarum. J Appl Microbiol 86:29–35

    CAS  PubMed  Google Scholar 

  75. O’Connor PM, Ross RP, Hill C, Cotter PD (2015) Antimicrobial antagonists against food pathogens: a bacteriocin perspective. Curr Opin Food Sci 2:51–57. https://doi.org/10.1016/j.cofs.2015.01.004

    Article  Google Scholar 

  76. O'Halloran FM, Morrissey SD, Murphy L, Thornton G, Shanahan F, O'Sullivan GC, Collins JK (1998) Adhesion of potential probiotic bacteria to human epithelial cell lines. Int Dairy J 8:596

    Google Scholar 

  77. Olaya Galán NN, Ulloa Rubiano JC, Velez Reyes FA, Fernandez Duarte KP, Salas Cardenas SP, Gutierrez Fernandez MF (2016) In vitro antiviral activity of Lactobacillus casei and Bifidobacterium adolescentis against rotavirus infection monitored by NSP 4 protein production. J Appl Microbiol 120:1041–1051

    PubMed  Google Scholar 

  78. Olivares M, Diaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonolla J, Navas M, Rodriguez JM, Xaus J (2007) Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 23:254–260

    CAS  PubMed  Google Scholar 

  79. Oliveira PM, Zannini E, Arendt EK (2014) Cereal fungal infection, mycotoxins, and lactic acid bacteriamediated bioprotection: fromcrop farming to cereal products. J Food Microbiol 37:78–95

    CAS  Google Scholar 

  80. Oliveira PM, Brosnan B, Furey A, Coffey A, Zannini E, Arendt EK (2015) Lactic acid bacteria bioprotection applied to the malting process. Part I: strain characterization and identification of antifungal compounds. Food Control 51:433–443

    CAS  Google Scholar 

  81. O’Sullivan L, Ross RP, Hill C (2003) A lacticin 481-producing adjunct culture increases starter lysis while inhibiting nonstarter lactic acid bacteria proliferation during cheddar cheese ripening. J Appl Microbiol 95:1235–1241

    PubMed  Google Scholar 

  82. Ouwehand AC, Forssten S, Hibberd AA, Lyra A, Stahl B (2016) Probiotic approach to prevent antibiotic resistance. Annals Med 48:246–255

    CAS  Google Scholar 

  83. Park MK, Vu NGO, Kwon YM, Lee YT, Yoo S, Cho YH, Hong SM, Hwang HS, Ko EJ, Jung YJ, Moon DW, Jeong EJ, Kim MC, Lee YN, Jang JH, Oh JS, Kim CH, Kang SM (2013) Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity. PLoS One 8:e75368

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Petruzzi L, Capozzi V, Berbegal C, Corbo MR, Bevilacqua A, Spano G, Sinigaglia M (2017) Microbial resources and enological significance: opportunities and benefits. Frontiers Microbiol 8:995–1007

    Google Scholar 

  85. Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, London, New York

    Google Scholar 

  86. Pothuraju R, Sharma RK (2018) Interplay of gut microbiota, probiotics in obesity: a review. Endocrine, metabolic & immune disorders-drug targets. Formerly Current Drug Targets-Immune Endocrine & Metabolic Disorders 18:212–220

    CAS  Google Scholar 

  87. Prabhurajeshwar C, Chandrakanth RK (2017) Probiotic potential of Lactobacilli with antagonistic activity against pathogenic strains: an in vitro validation for the production of inhibitory substances. Biom J 40:270–283

    Google Scholar 

  88. Pridmore RD, Pittet AC, Praplan F, Cavadini C (2008) Hydrogen peroxide production by Lactobacillus johnsonii NCC 533 and its role in anti-Salmonella activity. FEMS Microbiol Lett 283:210–215

    CAS  PubMed  Google Scholar 

  89. Ranadheera CS, Evans CA, Adams MC, Baines SK (2014) Effect of dairy probiotic combinations on in vitro gastrointestinal tolerance, intestinal epithelial cell adhesion and cytokine secretion. J Funct Foods 8:18–25

    CAS  Google Scholar 

  90. Rautava S, Salminen S, Isolauri E (2009) Specific probiotics in reducing the risk of acute infections in infancy a randomised, double-blind, placebo-controlled study. Br J Nutr 101:1722–1726

    CAS  PubMed  Google Scholar 

  91. Reid G (2008) Probiotic lactobacilli for urogenital health in women. J Clin Gastroenterol (Suppl 3, 42):234–236

  92. Reis JA, Paula AT, Casarotti SN, Penna ALB (2012) Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng Rev 4:124–140

    CAS  Google Scholar 

  93. Russo P, Caggianiello G, Arena MP, Fiocco D, Capozzi V, Spano G (2016) Lactic acid bacteria of fermented fruits and vegetables, In: Paramithiotis S, Lactic acid fermentation of fruits and vegetables: Taylor & Francis

  94. Russo P, Arena MP, Fiocco D, Capozzi V, Drider D, Spano G (2017) Lactobacillus plantarum with broad antifungal activity: a promising approach to increase safety and shelf-life of cereal-based products. Int J Food Microbiol 247:48–54

    CAS  PubMed  Google Scholar 

  95. Salva S, Nun˜ez M, Villena J, Ramo’n A, Font G, Alvarez S (2011) Development of a fermented goats’ milk containing Lactobacillus rhamnosus: in vivo study of health benefits J Sci Food Agric 91:2355–2362

    CAS  PubMed  Google Scholar 

  96. Leyva Salas M, Mounier J, Valence F, Coton M, Thierry A, Coton E (2017) Antifungal microbial agents for food biopreservation—a review. Microorganisms 5:37–90

    PubMed Central  Google Scholar 

  97. Sánchez-Hidalgo M, Montalbán-López M, Cebrián R, Valdivia E, Martínez-Bueno M, Maqueda M (2011) AS-48 bacteriocin: close to perfection. Cell Mol Life Sci 68:2845–2857. https://doi.org/10.1007/s00018-011-0724-4

    CAS  Article  PubMed  Google Scholar 

  98. Sandine WE, Thunell RK (2018) Types of starter cultures. In: Bacterial starter cultures for food, CRC Press, pp 127–144

  99. Santarmaki V, Kourkoutas Y, Zoumpopoulou G, Mavrogonatou E, Kiourtzidis M, Chorianopoulos N, Tassou C, Tsakalidou E, Simopoulos C, Ypsilantis P (2017) Survival, intestinal mucosa adhesion, and immunomodulatory potential of Lactobacillus plantarum strains. Current Microbiol 74:1061–1067

    CAS  PubMed  Google Scholar 

  100. Schiffrin EJ, Rochat F, Link-Amster H, Aeschlimann JM, Donnet-Hughes A (1994) Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. J Dairy Sci 78:491–497

    Google Scholar 

  101. Shornikova AV, Casas IA, Isolauri E, Vesikari T (1997) Lactobacillus reuteri as a therapeutic agent in acute diarrhoea in young children. J Pediatric Gastroenterol Nutrition 24:399–404

    CAS  Google Scholar 

  102. Seo BJ, Mun MR, RK J, Kim CJ, Lee I, Chang YH, Park YH (2010) Bile tolerant Lactobacillus reuteri isolated from pig feces inhibits enteric bacterial pathogens and porcine rotavirus. Vet Res Commun 34:323–333

    PubMed  Google Scholar 

  103. Sidooski T, Brandelli A, Bertoli SL, Souza CKD, Carvalho LFD (2018) Physical and nutritional conditions for optimized production of bacteriocins by lactic acid bacteria–a review. Critical Rev Food Sci Nutrition, (just-accepted), 1–26

  104. Silva CC, Silva SP, Ribeiro SC (2018) Application of bacteriocins and protective cultures in dairy food preservation. Frontiers Microbiol 9:594–608

    Google Scholar 

  105. Sjögren J, Magnusson J, Broberg A, Schnürer J, Kenne L (2003) Antifungal 3-hydroxy fatty acids from Lactobacillus plantarum MiLAB. J Appl Microbiol 69:7554–7557

    Google Scholar 

  106. Ström K, Sjögren J, Broberg A, Schnürer J (2002) Lactobacillus plantarum MiLAB produces the antifungal cyclic dipeptides cyclo (L-Phe-L-Pro) and cyclo (L-Phetrans- 4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microbiol 68:4322–4327

    PubMed  PubMed Central  Google Scholar 

  107. Suda S, Cotter PD, Hill C, Ross PR (2012) Lacticin 3147-biosynthesis, molecular analysis, immunity, bioengineering and applications. Curr Protein Pept Sci 13:193–204. https://doi.org/10.2174/138920312800785021

    CAS  Article  PubMed  Google Scholar 

  108. Šušković J, Kos B, Beganović J, Pavunc AL, Habjanič K, Matošić S (2010) Antimicrobial activity-the most important property of probiotic and starter lactic acid bacteria. Food Technol Biotechnol 48:296–307

    Google Scholar 

  109. Szajewska H, Mrukowicz JZ (2001) Probiotics in the treatment and prevention of acute infectious diarrhea in infants and children: a systematic review of published randomized, double-blind, placebo-controlled trials. J Pediatr Gastroenterol Nutr 33:S17–S25

    CAS  PubMed  Google Scholar 

  110. Tejero-Sariñena S, Barlow J, Costabile A, Gibson GR, Rowland I (2012) In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe 18:530–538

    PubMed  Google Scholar 

  111. Todorov SD, Wachsman MB, Knoetze H, Meincken M, Dicks LMT (2005) An antibacterial and antiviral peptide produced by Enterococcus mundtii ST4V isolated from soya beans. Int J Antimicrob Agents 25:508–513

    CAS  PubMed  Google Scholar 

  112. Tuomola EM, Ouwehand AC, Salminen SJ (1999) Human ileostomy glycoproteins as a model for small intestinal mucus to investigate adhesion of probiotics. Letters Appl Microbiol 28:159–163

    CAS  Google Scholar 

  113. Turner RB, Woodfolk JA, Borish L, Steinke JW, Patrie JT, Muehling LM, Lahtinen S, Lehtinen MJ (2017) Effect of probiotic on innate inflammatory response and viral shedding in experimental rhinovirus infection–a randomised controlled trial. Benefic Microbes 8:207–215

    CAS  Google Scholar 

  114. Tuyama AC, Cheshenko N, Carlucci MJ, Li JH, Goldberg CL, Waller DP, Anderson RA, Profy AT, Klotman ME, Keller MJ, Herold BC (2006) Acidform inactivates herpes simplex virus and prevents genital herpes in a mouse model: optimal candidate for microbicide combinations. J Infect Dis 194:795–803

    PubMed  Google Scholar 

  115. Twetman L, Larsen U, Fiehn NE, Stecksén-Blicks C, Twetman S (2009) Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. Acta Odontol Scand 67:284–288

    PubMed  Google Scholar 

  116. Valerio F, Lavemicocca P, Pascale M, Visconti A (2004) Production of phenyllactic acid by lactic acid bacteria: an approach to the selection of strains contributing to food quality and preservation. FEMS Microbiol Lett 23:289–295

    Google Scholar 

  117. Varyukhina S, Freitas M, Bardin S, Robillard E, Tavan E, Sapin C, Grill JP Trugnan G (2012) Glycanmodifying bacteria-derived soluble factors from Bacteroides thetaiotaomicron and Lactobacillus casei inhibit rotavirus infection in human intestinal cells. Microbes Infect 14:273–278

    CAS  PubMed  Google Scholar 

  118. Venema K, Venema G, Kok J (1995) Lactococcal bacteriocins: mode of action and immunity. Trends Microbiol 3:299–304

    CAS  PubMed  Google Scholar 

  119. Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther 40:277

    Google Scholar 

  120. Vijayaram S, Kannan S (2018) Probiotics: the marvelous factor and health benefits. Biomed Biotechnol Res J 2:1–8

    Google Scholar 

  121. Wang Z, Chai W, Burwinkel M, Twardziok S, Wrede P, Palissa C, Esch B, Schmid MFG (2013) Inhibitory influence of Enterococcus faecium on the propagation of swine influenza a virus in vitro. PLoS One 8:e53043

    CAS  PubMed  PubMed Central  Google Scholar 

  122. Wachsman MB, Farias ME, Takeda E, Sesma F, De Ruiz Holgado AP, de Torres RA, Coto CE (1999) Antiviral activity of enterocin CRL against herpes virus. Int J Antimicrob Agents 12:293–299

    CAS  PubMed  Google Scholar 

  123. Wachsman MB, Castilla V, De Ruiz Holgado AP, de Torres RA, Sesma F, Coto CE (2003) Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro. Antivir Res 58:17–24

    CAS  PubMed  Google Scholar 

  124. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, Levy Y (2004) Human immunodeficiency virus-driven expansion of CD4?CD25? regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 104:3249–3256

    CAS  PubMed  Google Scholar 

  125. Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, Yates M, Rollason TP, Young LS (2001) Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 357:1831–1836

    CAS  PubMed  Google Scholar 

  126. Woraprayote W, Malila Y, Sorapukdee S, Swetwiwathana A, Benjakul S, Visessanguan W (2016) Bacteriocins from lactic acid bacteria and their applications in meat and meat products. Meat Sci 120:118–132

    CAS  PubMed  Google Scholar 

  127. Woraprayote W, Pumpuang L, Tosukhowong A, Zendo T, Sonomoto K, Benjakul S, Visessanguan W (2018) Antimicrobial biodegradable food packaging impregnated with Bacteriocin 7293 for control of pathogenic bacteria in pangasius fish fillets. LWT 89:427–433

    CAS  Google Scholar 

  128. Yahfoufi N, Mallet JF, Graham E, Matar C (2018) Role of probiotics and prebiotics in immunomodulation. Curr Opin Food Sci 20:82–91

    Google Scholar 

Download references

Funding

This research was supported by the Apulian Region in the framework of Project “Biotecnologie degli alimenti per l’innovazione e la competitività delle principali filiere regionali: estensione della conservabilità e aspetti funzionali (BiotecA)”. Vittorio Capozzi was supported by Fondo di Sviluppo e Coesione 2007-2013—APQ Ricerca Regione Puglia “Programma regionale a sostegno della specializzazione intelligente e della sostenibilità sociale ed ambientale—FutureInResearch”.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Spano.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

The original version of this article was revised: The incorrect author name was captured as “Djamel Dridier” instead of “Djamel Drider”.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Arena, M.P., Capozzi, V., Russo, P. et al. Immunobiosis and probiosis: antimicrobial activity of lactic acid bacteria with a focus on their antiviral and antifungal properties. Appl Microbiol Biotechnol 102, 9949–9958 (2018). https://doi.org/10.1007/s00253-018-9403-9

Download citation

Keywords

  • Probiosis
  • Lactic acid bacteria
  • Antiviral
  • Antifungal