Abstract
Lactococcus lactis subsp. lactis bv. diacetylactis strains are often used as starter cultures by the dairy industry due to their production of acetoin and diacetyl, important substances that add buttery flavor notes in dairy products. Twenty-three L. lactis subsp. lactis isolates were obtained from dairy products (milk and cheese) and dairy farms (silage), identified at a biovar level, fingerprinted by rep-PCR and characterized for some technological features. Fifteen isolates presented molecular and phenotypical (diacetyl and citrate) characteristics coherent with L. lactis subsp. lactis bv. diacetylactis and rep-PCR allowed the identification of 12 distinct profiles (minimum similarity of 90%). Based on technological features, only two isolates were not able to coagulate skim milk and 10 were able to produce proteases. All isolates were able to acidify skim milk: two isolates, in special, presented high acidifying ability due to their ability in reducing more than two pH units after 24 h. All isolates were also able to grow at different NaCl concentrations (0 to 10%, w/v), and isolates obtained from peanut and grass silages presented the highest NaCl tolerance (10%, w/v). These results indicate that the L. lactis subsp. lactis bv. diacetylactis isolates presented interesting technological features for potential application in fermented foods production. Despite presenting promising technological features, the isolates must be assessed according to their safety before being considered as starter cultures.
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References
Carr FJ, Chill D, Maida N (2002) The lactic acid bacteria: a literature survey. Crit Rev Microbiol 28(4):281–370. https://doi.org/10.1080/1040-840291046759
Leroy F, De Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15(2):67–78. https://doi.org/10.1016/j.tifs.2003.09.004
Schleifer KH, Kraus J, Dvorak C, Kilpper-Bälz R, Collins MD, Fischer W (1985) Transfer of Streptococcus lactis and related Streptococci to the genus Lactococcus gen. nov. Syst Appl Microbiol 6(3):183–195. https://doi.org/10.1016/S0723-2020(85)80052-7
Nomura M, Kobayashi M, Narita T, Kimoto-Nira H, Okamoto T (2006) Phenotypic and molecular characterization of Lactococcus lactis from milk and plants. J Appl Microbiol 101(2):396–405. https://doi.org/10.1111/j.1365-2672.2006.02949.x
Dal Bello B, Cocolin L, Zeppa G, Field D, Cotter PD, Hill C (2012) Technological characterization of bacteriocin producing Lactococcus lactis strains employed to control Listeria monocytogenes in Cottage cheese. Int J Food Microbiol 153(1–2):58–65. https://doi.org/10.1016/j.ijfoodmicro.2011.10.016
Laroute V, Tormo H, Couderc C, Mercier-Bonin M, Le Bourgeois P, Cocaign-Bousquet M, Daveran-Mingot ML (2017) From genome to phenotype: an integrative approach to evaluate the biodiversity of Lactococcus lactis. Microorganisms 5(2):27. https://doi.org/10.3390/microorganisms5020027
Kempler GM, McKay LL (1981) Biochemistry and genetics of citrate utilization in Streptococcus lactis ssp. diacetylactis. J Dairy Sci 64(7):1527–1539. https://doi.org/10.3168/jds.s0022-0302(81)82721-x
García-Quintáns N, Repizo G, Martín M, Magni C, López P (2008) Activation of the diacetyl/acetoin pathway in Lactococcus lactis subsp. lactis bv. diacetylactis CRL264 by acidic growth. Appl Environ Microbiol 74(7):1988–1996. https://doi.org/10.1128/AEM.01851-07
Curioni PMG, Bosset JO (2002) Key odorants in various cheese types as determined by gas chromatography-olfactometry. Int Dairy J 12(12):959–984. https://doi.org/10.1016/S0958-6946(02)00124-3
Urbach G (1997) The flavour of milk and dairy products: II. Cheese: Contribution of volatile compounds. Int J Dairy Technol 50(3):79–89. https://doi.org/10.1111/j.1471-0307.1997.tb01743.x
Smit G, Smit BA, Engels WJM (2005) Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev 29(3 SPEC. ISS):591–610. https://doi.org/10.1016/j.femsre.2005.04.002
Deegan LH, Cotter PD, Hill C, Ross P (2006) Bacteriocins: biological tools for bio-preservation and shelf-life extension. Int Dairy J 16(9):1058–1071. https://doi.org/10.1016/j.idairyj.2005.10.026
Cotter PD, Ross RP, Hill C (2013) Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11(2):95–105. https://doi.org/10.1038/nrmicro2937
Delorme C, Godon JJ, Ehrlich SD, Renault P (1994) Mosaic structure of large regions of the Lactococcus lactis subsp. cremoris chromosome. Microbiology 140(11):3053–3060. https://doi.org/10.1099/13500872-140-11-3053
Beimfohr C, Ludwig W, Schleifer KH (1997) Rapid genotypic differentiation of Lactococcus lactis subspecies and biovar. Syst Appl Microbiol 20(2):216–221. https://doi.org/10.1016/S0723-2020(97)80068-9
Passerini D, Laroute V, Coddeville M, Le Bourgeois P, Loubière P, Ritzenthaler P, Cocaign-Bousquet M, Daveran-Mingot M-L (2013) New insights into Lactococcus lactis diacetyl- and acetoin-producing strains isolated from diverse origins. Int J Food Microbiol 160(3):329–336. https://doi.org/10.1016/j.ijfoodmicro.2012.10.023
Pu Z, Dobos M, Limsowtin G (2002) Integrated polymerase chain reaction-based procedures for the detection and identification of species and subspecies of the Gram-positive bacterial genus. J Appl :353–361.
Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ (2008) Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 74(8):2461–2470. https://doi.org/10.1128/AEM.02272-07
Kempler GM, McKay LL (1980) Improved medium for detection of citrate-fermenting Streptococcus lactis subsp. diacetylactis. Appl Environ Microbiol 39(4):926–927
Franciosi E, Settanni L, Cavazza A, Poznanski E (2009) Biodiversity and technological potential of wild lactic acid bacteria from raw cows’ milk. Int Dairy J 19(1):3–11. https://doi.org/10.1016/j.idairyj.2008.07.008
Dal Bello B, Rantsiou K, Bellio A, Zeppa G, Ambrosoli R, Civera T, Cocolin L (2010) Microbial ecology of artisanal products from North West of Italy and antimicrobial activity of the autochthonous populations. LWT Food Sci Technol 43(7):1151–1159. https://doi.org/10.1016/j.lwt.2010.03.008
Alves MP, Salgado RL, Eller MR, Vidigal PMP, Fernandes de Carvalho A (2016) Characterization of a heat-resistant extracellular protease from Pseudomonas fluorescens 07A shows that low temperature treatments are more effective in deactivating its proteolytic activity. J Dairy Sci 99(10):7842–7851. https://doi.org/10.3168/jds.2016-11236
Adams DM, Barach JT, Speck ML (1976) Effect of psychrotrophic bacteria from raw milk on milk proteins and stability of milk proteins to ultrahigh temperature treatment. J Dairy Sci 59(5):823–827. https://doi.org/10.3168/jds.S0022-0302(76)84282-8
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Psoni L, Kotzamanidis C, Yiangou M, Tzanetakis N, Litopoulou-Tzanetaki E (2007) Genotypic and phenotypic diversity of Lactococcus lactis isolates from Batzos, a Greek PDO raw goat milk cheese. Int J Food Microbiol 114(2):211–220. https://doi.org/10.1016/j.ijfoodmicro.2006.09.020
Kahala M, Mäki M, Lehtovaara A, Tapanainen JM, Katiska R, Juuruskorpi M, Juhola J, Joutsjoki V (2008) Characterization of starter lactic acid bacteria from the Finnish fermented milk product viili. J Appl Microbiol 105(6):1929–1938. https://doi.org/10.1111/j.1365-2672.2008.03952.x
Cavanagh D, Casey A, Altermann E, Cotter PD, Fitzgerald GF, McAuliffe O (2015) Evaluation of Lactococcus lactis isolates from nondairy sources with potential dairy applications reveals extensive phenotype-genotype disparity and implications for a revised species. Appl Environ Microbiol 81(12):3961–3972. https://doi.org/10.1128/AEM.04092-14
Siezen RJ, Bayjanov JR, Felis GE, van der Sijde MR, Starrenburg M, Molenaar D, Wels M, van Hijum SAFT, van Hylckama Vlieg JET (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. https://doi.org/10.1111/j.1751-7915.2011.00247.x
Domingos-Lopes MFP, Stanton C, Ross PR, Dapkevicius MLE, Silva CCG (2017) Genetic diversity, safety and technological characterization of lactic acid bacteria isolated from artisanal Pico cheese. Food Microbiol 63:178–190. https://doi.org/10.1016/j.fm.2016.11.014
Perin LM, Belviso S, Dal Bello B, Nero LA, Cocolin L (2017) Technological properties and biogenic amines production by bacteriocinogenic Lactococci and Enterococci strains isolated from raw goat’s milk. J Food Prot 80(1):151–157. https://doi.org/10.4315/0362-028x.jfp-16-267
Starrenburg M, Hugenholtz J (1991) Citrate fermentation by Lactococcus and Leuconostoc spp. Metab Clin Exp 57(12):3535–3540
Lucey JA, Johnson ME, Horne DS (2003) Invited review: perspectives on the basis of the rheology and texture properties of cheese. J Dairy Sci 86(9):2725–2743. https://doi.org/10.3168/jds.s0022-0302(03)73869-7
Piraino P, Zotta T, Ricciardi A, McSweeney PLH, Parente E (2008) Acid production, proteolysis, autolytic and inhibitory properties of lactic acid bacteria isolated from pasta filata cheeses: a multivariate screening study. Int Dairy J 18(1):81–92. https://doi.org/10.1016/j.idairyj.2007.06.002
Herreros MA, Fresno JM, González Prieto MJ, Tornadijo ME (2003) Technological characterization of lactic acid bacteria isolated from Armada cheese (a Spanish goats’ milk cheese). Int Dairy J 13(6):469–479. https://doi.org/10.1016/S0958-6946(03)00054-2
Liu M, Bayjanov JR, Renckens B, Nauta A, Siezen RJ (2010) The proteolytic system of lactic acid bacteria revisited: a genomic comparison. BMC Genomics 11(1):5–8. https://doi.org/10.1186/1471-2164-11-36
Tulini FL, Hymery N, Haertlé T, Le Blay G, De Martinis ECP (2016) Screening for antimicrobial and proteolytic activities of lactic acid bacteria isolated from cow, buffalo and goat milk and cheeses marketed in the southeast region of Brazil. J Dairy Res 83(1):115–124. https://doi.org/10.1017/S0022029915000606
Visser S (1993) Proteolytic enzymes and their relation to cheese ripening and flavor: an overview. J Dairy Sci 76(1):329–350. https://doi.org/10.3168/jds.s0022-0302(93)77354-3
González L, Sacristán N, Arenas R, Fresno JM, Eugenia Tornadijo M (2010) Enzymatic activity of lactic acid bacteria (with antimicrobial properties) isolated from a traditional Spanish cheese. Food Microbiol 27(5):592–597. https://doi.org/10.1016/j.fm.2010.01.004
Morandi S, Brasca M, Lodi R (2011) Technological, phenotypic and genotypic characterisation of wild lactic acid bacteria involved in the production of Bitto PDO Italian cheese. Dairy Sci Technol 91(3):341–359. https://doi.org/10.1007/s13594-011-0016-7
Zuljan FA, Mortera P, Alarcón SH, Blancato VS, Espariz M, Magni C (2016) Lactic acid bacteria decarboxylation reactions in cheese. Int Dairy J 62:53–62. https://doi.org/10.1016/j.idairyj.2016.07.007
Wouters JTM, Ayad EHE, Hugenholtz J, Smit G (2002) Microbes from raw milk for fermented dairy products. Int Dairy J 12(2–3):91–109. https://doi.org/10.1016/S0958-6946(01)00151-0
Deveau H, Labrie SJ, Chopin MC, Moineau S (2006) Biodiversity and classification of lactococcal phages. Appl Environ Microbiol 72(6):4338–4346. https://doi.org/10.1128/AEM.02517-05
Mahony J, Murphy J, Van Sinderen D (2012) Lactococcal 936-type phages and dairy fermentation problems: from detection to evolution and prevention. Front Microbiol 3(SEP):1–9. https://doi.org/10.3389/fmicb.2012.00335
Perin LM, Miranda RO, Todorov SD, Franco BDG d M, Nero LA (2014) Virulence, antibiotic resistance and biogenic amines of bacteriocinogenic lactococci and enterococci isolated from goat milk. Int J Food Microbiol 185:121–126. https://doi.org/10.1016/j.ijfoodmicro.2014.06.001
Lemay ML, Tremblay DM, Moineau S (2017) Genome engineering of virulent Lactococcal phages using CRISPR-Cas9. ACS Synth Biol 6(7):1351–1358. https://doi.org/10.1021/acssynbio.6b00388
Devirgiliis C, Zinno P, Perozzi G (2013) Update on antibiotic resistance in foodborne Lactobacillus and Lactococcus species. Front Microbiol 4:1–13. https://doi.org/10.3389/fmicb.2013.00301
Buňková L, Buňka F, Hlobilová M, Vaňátková Z, Nováková D, Dráb V (2009) Tyramine production of technological important strains of Lactobacillus, Lactococcus and Streptococcus. Eur Food Res Technol 229(3):533–538. https://doi.org/10.1007/s00217-009-1075-3
Flasarová R, Pachlová V, Buňková L, Menšíková A, Georgová N, Dráb V, Buňka F (2016) Biogenic amine production by Lactococcus lactis subsp. cremoris strains in the model system of Dutch-type cheese. Food Chem 194:68–75. https://doi.org/10.1016/j.foodchem.2015.07.069
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CNPq, CAPES (financial code 001), FAPEMIG, and CIRM-BIA for the concession of reference strains.
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Fusieger, A., Martins, M.C.F., de Freitas, R. et al. Technological properties of Lactococcus lactis subsp. lactis bv. diacetylactis obtained from dairy and non-dairy niches. Braz J Microbiol 51, 313–321 (2020). https://doi.org/10.1007/s42770-019-00182-3
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DOI: https://doi.org/10.1007/s42770-019-00182-3