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Antimicrobial Substances Including Bacteriocins Produced by Lactic Acid Bacteria Nagendrap Review Bioscience Microflora Vol. 21 (4), 217-223,2002 Antimicrobial Substances Including Bacteriocins Produced by Lactic Acid Bacteria NagendraP. SHAH1*and RajivDAVE2 SchoolofLife Sciences, Victoria University ofTechnology, POBox 14428, Melbourne CityMail Centre, Victoria 8001, Australia 2Currentaddress: Dairy Science Department , SouthDakota State University, Brookings, SD57007, USA Receivedforpublication, May9, 2002 Thisbrief overview highlights the antimicrobialsubstances including bacteriocins produced by lactic acid bacteria, witha particularemphasis on bacteriocinproduced by probioticbacteria, such as Lactobacillusacidophilus and bifidobacteria. Keywords: antimicrobialsubstances; bacteriocins; Lactobacillus acidophilus; bifidobacteria; nisin probiotic bacteria such as Lb. acidophilus and bifido- INTRODUCTION bacteria. A bacteriocin is defined as a proteinaceous compound ANTIMICROBIALSUBSTANCES PRODUCED produced by many different bacterial species that pos- BY DAIRY LACTIC ACID BACTERIA AND sess bactericidal action against other microorganisms, THEIR INHIBITORYSPECTRUM which are closely related to the producer organisms. A large number of bacterial species are reported to pro- Organic Acids duce bacteriocins including colicin from Escherichia Lactic acid bacteria while growing in milk produce coli, subtilin from Bacillus subtilis, pediocin by mainly lactic, formic, acetic, and propionic acids. These Pediococcus pentosaceus, and nisin from Lactococcus acids help lower the pH and create unfavourable envi- lactis subsp. lactis. The bacteriocins produced by spoil- ronment for other microorganisms. It has been demon- age and pathogenic group of microorganisms are not strated that bacteriostatic effect of lactic acid is pri- reviewed here, as they are precluded from food use due marily due to lactate anions rather than hydrogen ions. to the pathogenicity of producer organisms. In addi- The presence of lactic acid in fermented milk foods is tion to bacteriocins, lactic acid bacteria (LAB) produce shown to be inhibitory towards Staphylococcus and other antimicrobial substances such as lactic acid, Yersinia and bactericidal to Campylobacter and Sal- diacetyl, hydrogen peroxide, and bacteriocin-like in- monella. Lactic acid and/or propionic acid are effec- hibitory substances (5). LAB and the antimicrobial sub- tive against Campylobacter. Propionic acid produced stances produced by these bacteria have been used to by dairy propionibacteria has a broader inhibitory spec- produce safe and wholesome foods for centuries. The trum than lactic acid or acetic acid and inhibits moulds inhibitory activity of LAB leads to the creation of hos- and Gram-negative bacteria, but is ineffective against tile environment for food-borne pathogens and spoil- Gram-positive species. age organisms in foods.. The inhibition of pathogens and spoilage organisms is due to production of lactic Hydrogen Peroxide and other organic acids, hydrogen peroxide, diacetyl, Some strains of LAB including lactococci, lactoba- and bacteriocin, competition and nutrient depletion, and cilli, leuconostocs, and pediococci have the ability to altered redox potential. However, it is generally believed generate hydrogen peroxide during growth and lack of that the inhibitory activity is not a function of any one catalase by these bacteria causes its accumulation in compound, but it is a composite effect of several fac- growth media. Accumulation of hydrogen peroxide tors. This review will focus on the antimicrobial sub- occurs by the action of superoxide dismutase in most stances including bacteriocin produced by LAB, with lactic bacteria (particularly lactococci) or by manga- a particular emphasis on bacteriocins produced by nese ions present in high concentrations in the cyto- plasm of bacteria (particularly lactobacilli, leuconostocs *Corresponding author . Mailing address: School of Life Sciences, Victoria and pediococci). Lactococci produce sufficient hydro- University of Technology, PO Box 14428, Melbourne City Mail Centre, Victoria 8001, Australia. Phone: +61-3-9216-8289. Fax. +61-3-9216-8284. gen peroxide to be auto-inhibitory. Hydrogen peroxide E-mail: [email protected] has been reported to inhibit the growth of Staphylococ- 217 218 N.P. SHAH and R. DAVE cus aureus, E. coli, Salmonella typhimurium, Clostrid- so-called lantibiotics. Lantibiotics are small ribosomally ium perfringens, Pseudomonas sp. and other psy- synthesised polypeptides containing modified amino chrotrophs. However, the concentration of hydrogen acids such as lanthionine and 3-methyl-lanthionine. The peroxide produced by starters may not be sufficient to most prominent lantibiotic is nisin. Class I bacteriocin directly affect the microbial cells in foods. In raw milk, peptides undergo post-translational modifications. hydrogen peroxide generated by LAB can react with The class II bacteriocins are small hydrophobic and endogenous thiocyanate, a reaction catalysed by lac- heat-stable peptides, which do not contain unusual toperoxidase, to form intermediary oxidation products amino acids such as lanthionine. To date, many bacte- inhibitory to microorganisms. riocins belonging to class II have been identified and characterised such as Lactacin F, Lactococcin A, B and Diacetyl M, Leucosin, Plantaricin A, Pediocin PA-1, and Sakacin Diacetyl (2,3-butanedione) is a metabolic end prod- P, Curvacin A, Enterocin A. Class II bacteriocin pep- uct of LAB synthesised from the intermediary metabo- tides do not undergo post-translational modifications lite, pyruvate and is primarily known as flavour com- and contain between 30 and 60 residues. Class II bac- pound in fermented dairy products. Certain species of teriocins have two sub-groupings: class IIa bacterio- LAB have the ability to synthesise diacetyl, which can cins are effective against Listeria and thus have poten- inhibit yeasts, and several Gram-positive and Gram- tial as antimicrobial agent in food and feed. The major- negative organisms. The concentration required for such ity of bacteriocins produced by L. acidophilus are heat inhibition ranged from 100 to 400 ƒÊg/ml, while lactic stable, low molecular mass, non-lanthiobiotic peptides, starters produce only 10 to 80ƒÊg/ml of diacetyl . Thus, which belong to class II. The production of bacterio- diacetyl may be a minor contributor to the broad-spec- cins of Carnobacterium piscicola LV 17, Lb. plantarum trum antagonism. Cl 1 and Lactobacillus sake Lb 706 is induced by pep- tides excreted by producer cells. The peptides making Bacteriocins up the bacteriocin do not contain lanthionine residues Lactic acid bacteria produce a wide variety of anti- and such type of bacteriocin is the most prevalent bac- microbial proteins including peptide antibiotics, anti- teriocin produced by LAB. biotic-like substances, bacteriocins and bacteriocin-like Class III bacteriocins contain large heat labile pep- substances for the inhibition of food-borne pathogens tides (>30 kDa). A typical example is bacteriocin pro- and spoilage organisms. Among the antibiotic like sub- duced by L. helveticus, helveticin J. Class IV bacterio- stances, nisin is well characterised. Bacteriocins are cins are complex bacteriocins formed by the associa- proteinaceous compounds that show antimicrobial 'ac- tion of bactericidal proteins with one or more other es- tivity against closely related species' (7). While the sential chemical moieties such as lipid and carbohy- definition holds true for majority of bacteriocins, it is drate moieties. now evident that bacteriocins may act beyond closely Most bacteriocins produced by LAB have narrow an- related species or those confined to the same ecologi- tibacterial spectrum, confined to species related to pro- cal niche. ducer organisms, whereas some bacteriocins are active Among the bacteriocins, nisin is the one most exten- against Listeria sp. are and other food-borne pathogenic sively characterised and it is widely used as a food pre- and spoilage organisms. Most bacteriocins are hydro- servative in several countries. Other commercial prod- phobic and hence can be bound by lipids and phospho- ucts used by food industry include MicrogardTM (a prod- lipids. uct containing several metabolites produced by fermen- The antimicrobial activity of bacteriocins is due to tation with Propionibacterium freudenreichii subsp . increases in the permeability of the cytoplasmic mem- shermanii), which is used in cottage cheese. brane of target cells causing the dissipation of the pro- ton motive force or disturbing membrane transport and CLASSES OF BACTERIOCINS AND thus inhibiting energy production and biosynthesis of MODE OF ACTION proteins. The mechanism of action of nisin involves Biochemical and genetic studies of bacteriocins pro- binding to the peptidoglycan layer, causing destabilisa- duced by lactic acid bacteria have now defined four tion of the membrane by the formation of pores, which major classes (4). Bacteriocins of LAB belong to ei- allow leakage of ions such as potassium and magne- ther class I or class II. Class I bacteriocins are mem- sium and dissipation of the proton motive force. Gram- brane-active and heat-stable peptides. They contain the negative organisms are resistant to hydrophobic mol- ANTIMICROBIAL SUBSTANCES INCLUDING BACTERIOCINS PRODUCED BY LACTIC ACID BACTERIA 219 ecules like nisin due to outer membrane permeability licic acid column from an active fraction in the acid barrier. Nisin can be either bacteriostatic or bactericidal. soluble fraction of cultures of Lb. acidophilus.
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