Probiotic Lactococcus lactis: A Review

Lactococcus lactis plays a critical role in food, dairy and health sectors. In food and dairy industries, it is found in production processes of various fermented products such as sausages, pickled vegetables, beverages such as beer and wine, breads, soymilk kefir, sour milk, butter, cream, fresh cheese and different types of cheeses, like Cheddar, Colby, Cottage cheese, Camembert, cream cheese, Roquefort and Brie. Additionally, there is an increasing interest towards the possible health benefits of the probiotic activity of this organism which generally is species and strain specific and depends upon the survival in gastrointestinal tract with sufficient number. Certain strains have the ability to produce antimicrobial peptide called nisin which exhibits preservative potential. Therefore, application of bacteriocinogenic Lactococcus lactis in food and dairy sectors to preserve foods as a natural way and contributing health promoting attributes due to probiotic activity would definitely fulfil today’s consumer demands. This paper aimed to review the adaptation, antibiotic resistance, therapeutic and preservation potential of bacteriocinogenic and probiotic Lactococcus lac

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Aquilanti L, Silvestri G, Zannini E, Osimani A, Santarelli S, Clementi F. 2007. Phenotypic, genotypic and technological characterization of predominant lactic acid bacteria in Pecorino cheese from central Italy. J Appl Microbiol., 103:948-960.

Axelsson L. 1998. Lactic Acid Bacteria: Classification and Physiology. In: Lactic Acid Bacteria, Ed. Salminen S, von Wright A, Marcel Dekker, INC., New York, second edition 1- 73.

Bachmann H, Starrenburg MJC, Douwe Molenaar, Michiel Kleerebezem, van Hylckama Vlieg JET. 2012. Microbial domestication signatures of L. lactis can be reproduced by experimental evolution. Cold Spring Harbor Laboratory Press; ISSN 1088-9051/12; 22:115-124.

Bahey-El-Din M, Gahan CG. 2010. Lactococcus lactis: from the dairy industry to antigen and therapeutic protein delivery. Discov Med., 9(48):455-61.

Belen Florez A, Delgado S, Mayo B. 2005. Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can J Microbiol., 51:51-58.

Bermudez-Humaran LG, Cortes-Perez NG, Ah-Leung S, Lefevre F, Yang G, Pang Q, Wu C, Zeng Y, Adel-Patient K, Langella P. 2008. Current prophylactic and therapeutic uses of a recombinant Lactococcus lactis strain secreting biologically active interleukin-12. J Mol Microbiol Biotechnol., 14(1-3):80- 9.

Brusetti L, Borin S, Mora D, Rizzi A, Raddadi N, Sorlini C, Daffonchio D. 2006. Usefulness of length heterogeneity-PCR for monitoring lactic acid bacteria succession during maize ensiling. FEMS Microbiol Ecol., 56(1):154-64.

Campo N, Dias M, Daveran-Mingot ML, Ritzenthalter P, Le Bourgeois P. 2002. Genome plasticity in Lactococcus lactis. Antonie van Leeuwenhoek., 82:123-244.

Chan ES, Zhang Z. 2005. Bioencapsulation by compression coating of probiotic bacteria for their protection in an acidic medium. Process Biochem., 40:3346-3351.

Chung KT, Dickson JS, Crouse JD. 1989. Effect of nisin on growth of bacteria attached to meat. Appl Environ Microbiol., 55:1329- 1333.

Corich V, Mattiazzi A, Soldati E, Carraro A, Giaocomini A. 2005. Sau-PCR, a novel amplification technique for genetic fingerprinting of microorganisms, Appl Environ Microbiol., 71:6401-6406.

Corroler D, Mangin I, Desmasures N, Gueguen M. 1998. An ecological study of Lactococci isolated from raw milk in the Camembert cheese registered designation of origin area. Appl Environ Microbiol., 64:4729-4735.

D’Souza R, Pandeya DR, Hong ST. 2012. Review: Lactococcus lactis: An efficient Gram positive cell factory for the production and secretion of recombinant protein. Biomed Res, 23 (1):1-7.

De Man JC, Rogosa M, Sharpe ME. 1960. A medium for the cultivation of lactobacilli. J Appl Bacteriol., 23:130-135.

De Vuyst L. 1995. Nutritional factors affecting nisin production by Lactococcus lactis ssp. lactis NIZO 22186 in a synthetic medium. J Appl Bacteriol., 78:28-33.

De Vuyst L, Vandamme EJ. 1992. Influence of the carbon source on nisin production in Lactococcus lactis ssp. lactis batch fermentations. J Gen Microbiol., 138:571-578.

Delgado S, Mayo B. 2003. Phenotypic and genetic diversity of Lactococcus lactis and Enterococcus spp. strains isolated from Northern Spain starter-free farmhouse cheeses, Int J Fd Microbiol., 90:309-319.

Delves-Broughton J, Blackburn P, Evans RJ, Hugenholtz J. 1996. Applications of the bacteriocin, nisin. Antonie van Leeuwenhoek., 69:193-202.

Desmasures N, Gueguen M. 1997. Monitoring the microbiology of high quality milk by monthly sampling over 2 years. J Dairy Res., 64(2):271-280.

Deveau H, Moineau S. 2003. Use of RFLP to characterize Lactococcus lactis strains producing exopolysaccharides. J Dairy Sci., 86:1472-1475.

EI-Baradei A, Delacroix-Buchet JC, Ogier. 2008. Bacterial biodiversity of traditional Zabady fermented milk. Int J Fd Microbiol., 121:295-301.

FAO/WHO. 2002. Guidelines for the evaluation of probiotics in food, report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. London, ON, Canada.

Fernandez E, Alegria A, Delgado S, Mayo B. 2010. Phenotypic, genetic and technological characterization of Lactococcus garvieae strains isolated from a raw milk cheese. Int Dairy J., 20:142-148.

Galdeano C, de Moreno A, Vinderola G, Bibas Bonet ME, Perdigon G. 2007. A proposal model: mechanisms of immunomodulation induced by probiotic bacteria. Review. Clin Vacc Immunol., 14:485-492.

Gemelas L, Rigobello V, Ly-Chatain MH, Demarigny Y. 2013. Selective Lactococcus enumeration in raw milk. Fd Nutri Sci., 4:49-58.

Grattepanche F, Lacroix C, Audet P, Lapointe G. 2005. Quantification by real-time PCR of Lactococcus lactis ssp. cremoris in milk fermented by a mixed culture. Appl Microbiol Biotechnol., 66:414-421.

Harrigan FW, McCance EM. 1966. Laboratory methods in microbiology. Academic Press, London, New York: 285.

Huggins AM, Sandine WE. 1984. Differentiation of fast and slow milk coagulating isolates in strains of Streptococci. J Dairy Sci., 67(8):1674-1679.

Jenson PR, Hammer K. 1993. Minimal requirements for exponential growth of Lactococcus lactis. Appl Environ Microbiol., 59:4363-4366.

Khemariya P, Singh S, Nath G, Gulati AK. 2014. Diversity analysis, batch fermentation and characterization of nisin in identified strains of L. lactis spp. lactis. Fd Biotechnol., 28 (2):142-161.

Khemariya P, Singh S, Nath G, Gulati AK. 2013a. Isolation, identification, and antibiotic susceptibility of nis+ L. lactis from dairy and non-dairy sources. Czech J Fd Sci., 31(4):323-331.

Khemariya P, Singh S, Nath G, Gulati AK. 2013b. Development of a PCR-RFLP assay for the identification of L. lactis ssp. lactis and cremoris. Ann Microbiol., 63(1):109-115.

Khemariya P, Singh S, Nath G, Gulati AK. 2013c. Subspeciesspecific nested PCR assay for detection of L. lactis spp. lactis and L. lactis spp. cremoris. Fd Biotechnol., 27(3):222-234.

Khemariya P, Singh S, Nath G, Gulati AK. 2012. Diversity analysis of dairy and non-dairy strains of L. lactis ssp. lactis by multilocus sequence analysis (MLSA). Ann Microbiol., 63 (3):1065-1074.

Klaenhammer TR. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev., 12:39-86.

Le Loir Y, Azevedo V, Oliveira SC, Freitas DA, Miyoshi A, Bermudez-Humaran LG, Nouaille S, Ribeiro LA, Leclercq S, Gabriel JE, Guimaraes VD, Oliveira MN, Charlier C, Gautier M, Langella P. 2005. Protein secretion in Lactococcus lactis: an efficient way to increase the overall heterologous protein production. Microb Cell Fact., 4:2-13.

Lee MH, Roussel Y, Wilks M, Tabaqchali S. 2001. Expression of Helicobacter pylori urease subunit B gene in Lactococcus lactis MG1363 and its use as a vaccine delivery system against H. pylori infection in mice. Vaccine., 19(28-29):3927-35.

Li C, Ouyang F, Bai J. 2000. Extractive cultivation of Lactococcus lactis using a polyethylene glycol/MgSO4.7H2O aqueous two phase system to produce nisin. Biotechnol Lett., 22:843-847.

Liasi SA, Azmi TI, Hassan MD, Shuhaimi M, Rosfarizan M, Ariff AB. 2009. Antimicrobial activity and antibiotic sensitivity of three isolates of lactic acid bacteria from fermented fish product, Budu. Malay J Microbiol., 5:33–37.

Lindgren, Dobrogosz WJ. 1990. Antagonistic activities of lactic acid bacteria in food and feed fermentations, FEMS. Microbiol Rev., 87:149-164.

Makarova K, Slesarev A, Wolf Y, Sorokin A, Mirkin B, Koonin E, Pavlov A, Pavlova N, Karamychev V, Polouchine N, et al. 2006. Comparative genomics of the lactic acid bacteria. Proc Natl Acad Sci., 103:15611-15616.

Marui J, Boulom S, Panthavee W, Momma M, Kusumoto K, Nakahara K, Saito M. 2015. Culture-independent bacterial community analysis of the salty-fermented fish paste products of Thailand and Laos. Biosci Microbiota Fd Health., 34(2): 45- 52.

Maruo T, Gotoh Y, Nishimura H, Ohashi S, Toda T, Takahashi K. 2011. Oral administration of milk fermented with Lactococcus lactis ssp. cremoris FC protects mice against influenza virus infection. Lett Appl Microbiol., 55:135-140.

Miks-Krajnik M, Babuchowski A. 2014. 16S rRNA-targeted oligonucleotide probes for direct detection of Propionibacterium freudenreichii in presence of Lactococcus lactis with multicolour fluorescence in situ hybridization. Lett Appl Microbiol., 59(3):320-7.

Mrkonjić Fuka M, Engel M, Skelin A, Redžepović S, Schloter M. 2010. Bacterial communities associated with the production of artisanal Istrian cheese. Int J Fd Microbiol., 142:19-24.

Nouaille S, Ribeiro LA, Miyoshi A, Pontes D, Le Loir Y, Oliveira SC, Langella P, Azevedo V. 2003. Heterologous protein production and delivery systems for Lactococcus lactis. Genet Mol Res., 2:102-111.

Oelschlaeger TA. 2010. Mechanisms of probiotic actions-A review. Int J Med Microbiol., 300:57-62.

Otto R, ten Brink B, Veldkamp H, Konings WN. 1983. The relation between growth rate and electrochemical proton gradient of Streptococcus cremoris. FEMS Microbiol Lett., 16:69-74.

Pogačić T, Samaržija D, Corich V, Maura D, Kagkli DM, Giacomini A, et al. 2010. Microbiota of Karakačanski Skakutanac, an artisanal fresh sheep cheese studied by cultureindependent PCR-ARDRA and PCR-DGGE. Dairy Sci Technol., 90:461-468.

Poolman B, Konings WN. 1988. Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J Bacteriol., 170:700-707.

Pu ZY, Dobos M, Limsowtin GKY, Powell LB. 2002. Integrated polymerase chain reaction-based procedures for the detection and identification of species and subspecies of the Gram positive bacterial genus Lactococcus. J Appl Microbiol., 93:353-361.

Que´ne´e, P, Lepage E, Scott Kim W, Vegnagud G, Gruss A. 2005. Minisatellite polymorphism as a tool to distinguish closely related Lactococcus lactis strain. FEMS Microbiol Lett., 248:101-109.

Quiberoni A, Rezaiki L, El Karoui M, Biswas I, Tailliez P, Gruss A. 2001. Distinctive features of homologous recombination in an ‘old’ microorganism Lactococcus lactis. Res Microbiol., 152: 131-139.

Rademarker JLW, Herbet H, Starrenburg MJC, Naser SM, Gevers D, Kelly WJ, Hugenholtz J, Swings J, Vlirg JET. 2007.

Diversity analysis of dairy and non-dairy Lactococcus lactis isolates using a novel multilocus sequence analysis scheme and (GTG)5-PCR fingerprinting. Appl Environ Microbiol., 73:7128- 7137.

Ribeiro LA, Azevedo V, Le Loir Y, Oliveira SC, Dieye Y, Piard JC, Gruss A, Langella P. 2002. Production and targeting of the Brucella abortus antigen L7/L12 in Lactococcus lactis: a first step towards food-grade live vaccines against brucellosis. Appl Environ Microbiol., 68(2):910-916.

Robinson K, Chamberlain LM, Schofield KM, Wells JM, Le Page RW. 1997. Oral vaccination of mice against tetanus with recombinant Lactococcus lactis. Nat Biotechnol., 15(7):653-657.

Roissart H, Luquet. 1994. Lactic acid bacteria: fundamental and technological aspects. Uriage, Lorica, France 1:605. ISBN 2 9507477 0 1.

Ross RP, Morgan S, Hill C. 2002. Preservation and fermentation: past, present and future. Int J Fd Microbiol., 79:3-16.

Ruggirello M, Dolci P, Cocolin L. 2014. Detection and Viability of Lactococcus lactis throughout Cheese Ripening. PLOS ONE doi: 10.1371/journal.pone.0114280

Salbi RA, Serhan M, Bassil M. 2014. Molecular verification of two potent bacteria isolated from Darfiyeh cheese: Lactococcus lactis ssp. lactis and Lactobacillus plantarum. Adv Microbiol., 4: 609-615.

Salyers AA, Gupta A, Wang Y. 2004. Human intestinal bacteria as reservoirs for antibiotic resistance genes. Trends Microbiol., 12:412-416.

Samaržija D, Sikora S, Redžepović S, Antunac N, Havranek J. 2002. Application of RAPD analysis for identification of Lactococcus lactis ssp. cremoris strains isolated from artisanal cultures. Microbiol Res., 157:13-17.

Sanchez C, Neves AR, Cavalheiro J, Santos MM, dos GarciaQuintans N, Lopez P, Santos H. 2008. Contribution of citrate metabolism to the growth of Lactococcus lactis CRL264 at low pH. Appl Environ Microbiol., 74:1136-1144.

Saubusse M, Millet L, Delbès C, Callon C, Montel MC. 2007.

Application of single strand conformation polymorphism -PCR method for distinguishing cheese bacterial communities that inhibit Listeria monocytogenes. Int J Food Microbiol., 116(1):126-35.

Savoie S, Champagne CP, Chiasson S, Audet P. 2007. Media and process parameters affecting the growth, strain ratios and specific acidifying activities of a mixed lactic starter containing aroma-producing and probiotic strains. J Appl Microbiol., 103:163-174

Schleifer KH, Kraus J, Dvorak C, Klipper-Balz R, Collins MD, Fisher W. 1985. Transfer of Streptococcus lactis and related streptococci to the genus Lactococcus gen. nov. Sys Appl Microbiol., 6:183-195.

Siezen RJ, Bayjanov JR, Felis GE, van der Sijde MR, Starrenburg M, Molenaar D, Wels M, van Hijum SA, van Hylckama Vlieg JE. 2011. Genome-scale diversity and niche adaptation analysis of Lactococcus lactis by comparative genome hybridization using multi-strain arrays. Microb Biotechnol., 4(3):383-402.

Siezen RJ, Starrenburg MJC, Boekhorst J, Renckens B, Molenaar D, van Hylckama Vlieg JET. 2008. Genome-scale genotypephenotype matching of two Lactococcus lactis isolates from plants identifies mechanisms of adaptation to the plant niche. Appl Environ Microbiol., 74(2):424-436.

Siezen RJ, Renckens B, van Swam I, Peters S, van Kranenburg R, Kleerebezem M, de Vos WM. 2005. Complete sequences of four plasmids of Lactococcus lactis ssp. cremoris SK11 reveal extensive adaptation to the dairy environment. Appl Environ Microbiol., 71: 8371-8382.

Stiles MA, Holzapfel WH. 1997. Lactic acid bacteria of food and their current taxonomy. Int J Fd Microbiol., 36:1-29.

Suganthi V, Selvarajan E, Subathradevi C, Mohanasrinivasan V. 2012. Lantibiotic nisin: Natural preservative from Lactococcus lactis. Int res J Pharma., 3 (1):13-19.

Suskovic J, Kos B, Beganovic J, Pavunc AL, Habjanic K, Matosic S. 2010. Antimicrobial Activity- The most important property of probiotic and starter lactic acid bacteria. Fd Technol Biotechnol., 48(3):296-307.

Taïbi A, Dabour N, Lamoureux M, Roy D, La Pointe G. 2010. Evaluation of the genetic polymorphism among Lactococcus lactis ssp. cremoris strains using comparative genomic hybridization and multilocus sequence analysis. Int J Fd Microbiol., 144:20-28.

Tanous C, Kieronczyk A, Helinck S, Chambellon E, Yvon M. 2002.

Glutamate dehydrogenase activity: a major criterion for the selection of flavour-producing lactic acid bacteria strains. Antonie Leeuwenhoek., 82:271–278.

Temmerman R, Scheirlinck I, Huys G, Swings J. 2003. Culture-- independent analysis of probiotic products by denaturing gradient gel electrophoresis. Appl Environ Microbiol., 69:220- 226.

Terzaghi BE, Sandine WE. 1975. Improved medium for lactic streptococci and their bacteriophages. J Appl Microbiol., 29:807-813.

Teuber M. 1999. Spread of antibiotic resistance with food-borne pathogens. Cell Mol Life Sci., 56:755-763.

Todorov SD, Furtado DN, Saad SMI, Tome E, Franco BDGM. 2011. Potential beneficial properties of bacteriocin-producing lactic acid bacteria isolated from smoked salmon. J Appl Microbiol., 110(4):971-986.

Tornadijo ME, Fresno JM, Bernardo A, Martin Sarmiento R, Carballo J. 1995. Microbiological changes throughout the manufacturing and ripening of a Spanish goat’s raw milk cheese (Armada variety). Lait, 75:551-570.

Turner WE, Sandine PR, Elliker, Day EA. 1963.Use of tetrazolium dyes in an agar medium for differentiation of Streptococcus lactis and S. cremoris. J Dairy Sci., 46(5):380-385.

Waes. 1968. The enumeration of Aroma bacteria in BD starters. Neth Milk Dairy J., 22:29-39.

Wells JM, Mercenier A. 2008. Mucosal delivery of therapeutic and prophylactic molecules using lactic acid bacteria. Nat Rev Microbiol, 6(5):349-362.

Wold AE, Dahlgren UI, Hanson LA, Mattsby-Baltzer I, Midvetdt T. 1989. Difference between bacterial and food antigens in mucosal immunogenicity. Infect Immun., 57(9):2666-2673.

Zhou JS, Pillidge CJ, Gopal PK, Gill HS. 2005. Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Fd Microbiol., 98:211-217.