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.
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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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Champagne CP, Fustier P (2007) Microencapsulation for the improved delivery of bioactive compounds into foods. Curr Opin Biotechnol 18:184–190
Chen H, Hoover DG (2003) Bacteriocins and their food applications. Compr Rev Food Sci Food Saf 2:82–100
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
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
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
Conti C, Malacrino C, Mastromarino P (2009) Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J Physiol Pharmacol 6:19–26
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
Cotter PD, Hill C, Ross RP (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3:777–788
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
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
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
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
Diener M (2016) Roadblock for antigens – take a detour via M cells. Acta Physiol 216:13–14. https://doi.org/10.1111/apha.12595
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
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
Garrity GM, Holt JG (2001) The road map to the manual. In: Bergey’s manual® of systematic bacteriology. Springer, New York, pp 119–166
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
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
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
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
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
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
Héchard Y, Sahl HG (2002) Mode of action of modified and unmodified bacteriocins from Gram-positive bacteria. Biochimie 84:545–557
Hathout AS, Ali SE (2014) Biological detoxification of mycotoxins: a review. Annals Microbiol 64(3):905–919
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
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
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
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
Jyoti B, Suresh AK, Venkatesh K (2003) Diacetyl production and growth of Lactobacillus rhamnosus on multiple substrates. World J Microbiol Biotechnol 19:509–515
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
Karlovsky P (1999) Biological detoxification of fungal toxins and its use in plant breeding, feed and food production. Nat Toxins 7:1–23
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
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
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
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
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
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
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
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
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
López-Cuellar MDR, Rodríguez-Hernández AI, Chavarría-Hernández N (2016) LAB bacteriocin applications in the last decade. Biotechnol Biotechnol Equipment 30:1039–1050
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
Malhotra B, Keshwani A, Kharkwal H (2015) Antimicrobial food packaging: potential and pitfalls. Frontiers Microbiol 6:611–619
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
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
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
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
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
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
McCormick SP (2013) Microbial detoxification of mycotoxins. J Chemical Ecol 39(7):907–918
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
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
Mombelli B, Gismondo MR (2000) The use of probiotics in medical practice. Int J Antimicrob Agents 16:531–536
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
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
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
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
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
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
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
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
Ouwehand AC, Forssten S, Hibberd AA, Lyra A, Stahl B (2016) Probiotic approach to prevent antibiotic resistance. Annals Med 48:246–255
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
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
Pitt JI, Hocking AD (2009) Fungi and food spoilage. Springer, London, New York
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
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
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
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
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
Reid G (2008) Probiotic lactobacilli for urogenital health in women. J Clin Gastroenterol (Suppl 3, 42):234–236
Reis JA, Paula AT, Casarotti SN, Penna ALB (2012) Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng Rev 4:124–140
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
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
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
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
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
Sandine WE, Thunell RK (2018) Types of starter cultures. In: Bacterial starter cultures for food, CRC Press, pp 127–144
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
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
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
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
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
Silva CC, Silva SP, Ribeiro SC (2018) Application of bacteriocins and protective cultures in dairy food preservation. Frontiers Microbiol 9:594–608
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
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
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
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
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
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
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
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
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
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
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
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
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
Venema K, Venema G, Kok J (1995) Lactococcal bacteriocins: mode of action and immunity. Trends Microbiol 3:299–304
Ventola CL (2015) The antibiotic resistance crisis: part 1: causes and threats. Pharm Ther 40:277
Vijayaram S, Kannan S (2018) Probiotics: the marvelous factor and health benefits. Biomed Biotechnol Res J 2:1–8
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
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
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
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
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
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
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
Yahfoufi N, Mallet JF, Graham E, Matar C (2018) Role of probiotics and prebiotics in immunomodulation. Curr Opin Food Sci 20:82–91
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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”.
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The original version of this article was revised: The incorrect author name was captured as “Djamel Dridier” instead of “Djamel Drider”.
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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
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DOI: https://doi.org/10.1007/s00253-018-9403-9