Acta NaturaeActa NaturaeActa Naturae2075-8251Acta Naturae Ltd2774710.32607/actanaturae.27747Research ArticlesЭкспериментальные статьиResearch ArticleComprehensive characterization of five Lactococcus strains: from phenotypic traits to genomic featuresКомплексная характеристика пяти штаммов Lactococcus: от фенотипических свойств к геномным особенностямhttps://orcid.org/0009-0002-1139-6162AntipenkoIvan D.АнтипенкоИван Денисович
Russian Federation

Laboratory for Research on Molecular Mechanisms of Longevity, Department of Biology and Biotechnology

факультет биологии и биотехнологии, лаборатория исследований молекулярных механизмов долголетия

iantipenko@hse.ruhttps://orcid.org/0000-0002-1108-3695SorokinaNinel P.СорокинаНинель Петровна
Russian Federation
n.sorokina@fncps.ruhttps://orcid.org/0000-0001-8251-992XKucherenkoIrina V.КучеренкоИрина Валентиновна
Russian Federation
i.kucherenko@fncps.ruhttps://orcid.org/0000-0002-0710-3083KuraevaElena V.КураеваЕлена Вячеславовна
Russian Federation
e.kuraeva@fncps.ruhttps://orcid.org/0000-0002-1381-9344MasezhnayaElena S.МасежнаяЕлена Сергеевна
Russian Federation
e.masezhnaya@fncps.ruhttps://orcid.org/0000-0002-6668-5028ShkurnikovMaxim Y.ШкурниковМаксим Юрьевич
Russian Federation

Laboratory for Research on Molecular Mechanisms of Longevity, Department of Biology and Biotechnology

факультет биологии и биотехнологии, лаборатория исследований молекулярных механизмов долголетия

mshkurnikov@hse.ruHSE UniversityНациональный исследовательский университет «Высшая школа экономики»All-Russian Research Institute of Butter and Cheese Making, Branch of the Gorbatov Federal Research Center for Food SystemsВсероссийский научно-исследовательский институт маслоделия и сыроделия – филиал Федерального научного центра пищевых систем им. В.М. Горбатова РАН0412202517483921607202521082025Copyright ©; 2025, Antipenko I.D., Sorokina N.P., Kucherenko I.V., Kuraeva E.V., Masezhnaya E.S., Shkurnikov M.Y.Copyright ©; 2025, Антипенко И.Д., Сорокина Н.П., Кучеренко И.В., Кураева Е.В., Масежная Е.С., Шкурников М.Ю.2025Antipenko I.D., Sorokina N.P., Kucherenko I.V., Kuraeva E.V., Masezhnaya E.S., Shkurnikov M.Y.Антипенко И.Д., Сорокина Н.П., Кучеренко И.В., Кураева Е.В., Масежная Е.С., Шкурников М.Ю.https://creativecommons.org/licenses/by/4.0https://actanaturae.ru/2075-8251/article/view/27747

The efficiency of dairy product fermentation directly depends on the properties of the lactic acid bacteria used, particularly on their metabolic activity and resistance to bacteriophages. Therefore, an understanding of the relationships between the genetic and phenotypic traits of industrial strains is of elevated importance. In this study, we comprehensively analyzed five Lactococcus strains widely used in the Russian dairy industry, combining whole-genome sequencing with phenotypic profiling. Despite the fact of genetic similarity among four of the L. lactis strains, we still identified significant differences in their metabolic activity. Comparative structural analysis of previously published genomes of 337 L. lactis and 147 L. cremoris strains revealed species-specific features of the lactose metabolism; in particular, the absence of the lacZ gene in L. cremoris. Notably, prophages were found in three of the studied strains, which was in correlation with their reduced acidification activity. L. lactis FNCPS 51n and 73n strains displayed resistance to all 50 tested bacteriophages, which may be associated with the presence of the AbiB abortive infection system. These findings underscore the importance of integrating genomic and phenotypic analyses when selecting efficient and phage-resistant Lactococcus starters in the dairy industry.

Эффективность ферментации молочных продуктов зависит от характеристик молочнокислых бактерий, прежде всего от их метаболической активности и устойчивости к бактериофагам, поэтому важно понимать связь между генетическими и фенотипическими особенностями штаммов, используемых в промышленности. Нами проведен комплексный анализ пяти широко применяемых в России штаммов Lactococcus с использованием полногеномного секвенирования и оценки фенотипических свойств. Несмотря на генетическое сходство четырех штаммов L. lactis, выявлены значительные различия в их метаболической активности. Сравнение структуры ранее опубликованных геномов 337 штаммов L. lactis и 147 штаммов L. cremoris выявило отсутствие гена lacZ у L. сremoris, что указывает на видоспецифичные особенности метаболизма лактозы. Важно отметить, что у трех из пяти исследованных штаммов было выявлено наличие профагов, что коррелировало с пониженной кислотообразующей активностью. Штаммы L. lactis FNCPS 51n и 73n были устойчивыми ко всем 50 протестированным бактериофагам, что может быть связано с наличием системы абортивной инфекции AbiB. Полученные данные подчеркивают значимость интеграции геномного и фенотипического анализа при отборе эффективных и устойчивых стартовых культур Lactococcus для молочной промышленности.

Lactococcusfermentationgenomic profilingprophagesstarter culturesbacteriophagesLactococcusfermentationgenomic profilingprophagesstarter culturesbacteriophagesМинистерство науки и высшего образования РФMinistry of Science and Higher Education of the Russian Federation075-15-2024-483Kondrotiene K, Zavistanaviciute P, Aksomaitiene J, Novoslavskij A, Malakauskas M. Lactococcus lactis in dairy fermentation—Health-promoting and probiotic properties. Fermentation. 2023;10(1):16. doi: 10.3390/fermentation10010016Kondrotiene K, Zavistanaviciute P, Aksomaitiene J, Novoslavskij A, Malakauskas M. Lactococcus lactis in dairy fermentation—Health-promoting and probiotic properties. Fermentation. 2023;10(1):16.Li TT, Tian WL, Gu CT. Elevation of Lactococcus lactis subsp. cremoris to the species level as Lactococcus cremoris sp. nov. and transfer of Lactococcus lactis subsp. tructae to Lactococcus cremoris as Lactococcus cremoris subsp. tructae comb. nov. Int J Syst Evol Microbiol. 2021;71(3):004727. doi: 10.1099/ijsem.0.004727Li TT, Tian WL, Gu CT. Elevation of Lactococcus lactis subsp. cremoris to the species level as Lactococcus cremoris sp. nov. and transfer of Lactococcus lactis subsp. tructae to Lactococcus cremoris as Lactococcus cremoris subsp. tructae comb. nov. Int J Syst Evol Microbiol. 2021;71(3):004727.Torres Manno M, Zuljan F, Alarcón S, et al. Genetic and phenotypic features defining industrial relevant Lactococcus lactis, L. cremoris and L. lactis biovar. diacetylactis strains. J Biotechnol. 2018;282:25-31. doi: 10.1016/j.jbiotec.2018.06.345Torres Manno M, Zuljan F, Alarcón S, et al. Genetic and phenotypic features defining industrial relevant Lactococcus lactis, L. cremoris and L. lactis biovar. diacetylactis strains. J Biotechnol. 2018;282:25-31. doi: https://doi.org/10.1016/j.jbiotec.2018.06.345Kim WS, Ren J, Dunn NW. Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol Lett. 1999;171(1):57-65. doi: 10.1111/j.1574-6968.1999.tb13412.xKim WS, Ren J, Dunn NW. Differentiation of Lactococcus lactis subspecies lactis and subspecies cremoris strains by their adaptive response to stresses. FEMS Microbiol Lett. 1999;171(1):57-65.van Mastrigt O, Mager EE, Jamin C, Abee T, Smid EJ. Citrate, low pH and amino acid limitation induce citrate utilization in Lactococcus lactis biovar diacetylactis. Microb Biotechnol. 2018;11(2):369-380. doi: 10.1111/1751-7915.13031van Mastrigt O, Mager EE, Jamin C, Abee T, Smid EJ. Citrate, low pH and amino acid limitation induce citrate utilization in Lactococcus lactis biovar diacetylactis. Microb Biotechnol. 2018;11(2):369-380.Curioni PMG, Bosset JO. Key odorants in various cheese types as determined by gas chromatography-olfactometry. Int Dairy J. 2002;12(12):959-984. doi: 10.1016/s0958-6946(02)00124-3Curioni PMG, Bosset JO. Key odorants in various cheese types as determined by gas chromatography-olfactometry. Int Dairy J. 2002;12(12):959-984.Castellone V, Bancalari E, Rubert J, Gatti M, Neviani E, Bottari B. Eating fermented: Health benefits of LAB-fermented foods. Foods. 2021;10(11):2639. doi: 10.3390/foods10112639Castellone V, Bancalari E, Rubert J, Gatti M, Neviani E, Bottari B. Eating fermented: Health benefits of LAB-fermented foods. Foods. 2021;10(11):2639.Poudel R, Thunell RK, Oberg CJ, et al. Comparison of growth and survival of single strains of Lactococcus lactis and Lactococcus cremoris during Cheddar cheese manufacture. J Dairy Sci. 2022;105(3):2069-2081. doi: 10.3168/jds.2021-20958Poudel R, Thunell RK, Oberg CJ, et al. Comparison of growth and survival of single strains of Lactococcus lactis and Lactococcus cremoris during Cheddar cheese manufacture. J Dairy Sci. 2022;105(3):2069-2081. doi: https://doi.org/10.3168/jds.2021-20958Kelleher P, Mahony J, Bottacini F, Lugli GA, Ventura M, van Sinderen D. The Lactococcus lactis Pan-Plasmidome. Front Microbiol. 2019;10:707. doi: 10.3389/fmicb.2019.00707Kelleher P, Mahony J, Bottacini F, Lugli GA, Ventura M, van Sinderen D. The Lactococcus lactis Pan-Plasmidome. Front Microbiol. 2019;Volume 10-2019. https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2019.00707Panebianco F, Giarratana F, Caridi A, Sidari R, De Bruno A, Giuffrida A. Lactic acid bacteria isolated from traditional Italian dairy products: Activity against Listeria monocytogenes and modelling of microbial competition in soft cheese. Lwt. 2021;137:110446. doi: 10.1016/j.lwt.2020.110446Panebianco F, Giarratana F, Caridi A, Sidari R, De Bruno A, Giuffrida A. Lactic acid bacteria isolated from traditional Italian dairy products: Activity against Listeria monocytogenes and modelling of microbial competition in soft cheese. Lwt. 2021;137:110446.Tomovska J, Gjorgievski N, Makarijoski B. Examination of pH, titratable acidity and antioxidant activity in fermented Milk. J Mater Sci Eng A. 2016;6(11-12):326-333. doi: 10.17265/2161-6213/2016.11-12.006Tomovska J, Gjorgievski N, Makarijoski B. Examination of pH, titratable acidity and antioxidant activity in fermented Milk. J Mater Sci Eng A. 2016;6(11):326-333.Gutierrez-Mendez N, Rodríguez-Figueroa JC, Gonzalez-Cordova AF, Nevarez-Moorillon GV, Rivera-Chavira B, Vallejo-Cordoba B. Phenotypic and genotypic characteristics of Lactococcus lactis strains isolated from different ecosystems. Can J Microbiol. 2010;56(5):432-439. doi: 10.1139/w10-026Gutierrez-Mendez N, Rodríguez-Figueroa JC, Gonzalez-Cordova AF, Nevarez-Moorillon G V, Rivera-Chavira B, Vallejo-Cordoba B. Phenotypic and genotypic characteristics of Lactococcus lactis strains isolated from different ecosystems. Can J Microbiol. 2010;56(5):432-439.Kutter E. Phage host range and efficiency of plating. Methods Mol Biol. 2009;501:141-149. doi: 10.1007/978-1-60327-164-6_14Kutter E. Phage host range and efficiency of plating. Bacteriophages: Methods and protocols, Volume 1: Isolation, characterization, and interactions. Published online 2009:141-149.Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics. 2020;70(1):e102. doi: 10.1002/cpbi.102Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics. 2020;70(1):e102.Langdon WB. Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. BioData Min. 2015;8(1):1. doi: 10.1186/s13040-014-0034-0Langdon WB. Performance of genetic programming optimised Bowtie2 on genome comparison and analytic testing (GCAT) benchmarks. BioData Min. 2015;8:1-7.Li H, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078-2079. doi: 10.1093/bioinformatics/btp352Li H, Handsaker B, Wysoker A, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078-2079.Walker BJ, Abeel T, Shea T, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963. doi: 10.1371/journal.pone.0112963Walker BJ, Abeel T, Shea T, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963.Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-1075. doi: 10.1093/bioinformatics/btt086Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-1075.Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. Methods Mol Biol. 2019;1962:227-245. doi: 10.1007/978-1-4939-9173-0_14Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. Gene prediction: methods and protocols. Published online 2019:227-245.Tatusova T, DiCuccio M, Badretdin A, et al. NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res. 2016;44(14):6614-6624. doi: 10.1093/nar/gkw569Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J Mol Biol. 2016;428(4):726-731. doi: 10.1016/j.jmb.2015.11.006Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. J Mol Biol. 2016;428(4):726-731. doi: https://doi.org/10.1016/j.jmb.2015.11.006Olson RD, Assaf R, Brettin T, et al. Introducing the Bacterial and Viral Bioinformatics Resource Center (BV-BRC): a resource combining PATRIC, IRD and ViPR. Nucleic Acids Res. 2023;51(D1):D678-D689. doi: 10.1093/nar/gkac1003Wishart DS, Han S, Saha S, et al. PHASTEST: faster than PHASTER, better than PHAST. Nucleic Acids Res. 2023;51(W1):W443-W450. doi: 10.1093/nar/gkad382Tesson F, Planel R, Egorov AA, et al. A Comprehensive Resource for Exploring Antiphage Defense: DefenseFinder Webservice,Wiki and Databases. Peer Community J. 2024;4:e91. doi: 10.24072/pcjournal.470Tesson F, Planel R, Egorov AA, et al. A Comprehensive Resource for Exploring Antiphage Defense: DefenseFinder Webservice,Wiki and Databases. Peer Community Journal. 2024;4:e91. doi: 10.24072/pcjournal.470Couvin D, Bernheim A, Toffano-Nioche C, et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res. 2018;46(W1):W246-W251. doi: 10.1093/nar/gky425Carattoli A, Zankari E, García-Fernández A, et al. In Silico Detection and Typing of Plasmids using PlasmidFinder and Plasmid Multilocus Sequence Typing. Antimicrob Agents Chemother. 2014;58(7):3895-3903. doi: 10.1128/aac.02412-14Alessandra C, Ea Z, Aurora GF, et al. In Silico Detection and Typing of Plasmids using PlasmidFinder and Plasmid Multilocus Sequence Typing. Antimicrob Agents Chemother. 2014;58(7):3895-3903. doi: 10.1128/aac.02412-14Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics. 2016;32(6):929-931. doi: 10.1093/bioinformatics/btv681Lee I, Ouk Kim Y, Park SC, Chun J. OrthoANI: An improved algorithm and software for calculating average nucleotide identity. Int J Syst Evol Microbiol. 2016;66(2):1100-1103. doi: 10.1099/ijsem.0.000760Kieliszek M, Pobiega K, Piwowarek K, Kot AM. Characteristics of the proteolytic enzymes produced by lactic acid bacteria. Molecules. 2021;26(7):1858. doi: 10.3390/molecules26071858Kieliszek M, Pobiega K, Piwowarek K, Kot AM. Characteristics of the proteolytic enzymes produced by lactic acid bacteria. Molecules. 2021;26(7):1858.Passerini D, Beltramo C, Coddeville M, et al. Genes but Not Genomes Reveal Bacterial Domestication of Lactococcus Lactis. PLoS One. 2010;5(12):e15306. doi: 10.1371/journal.pone.0015306Passerini D, Beltramo C, Coddeville M, et al. Genes but Not Genomes Reveal Bacterial Domestication of Lactococcus Lactis. PLoS One. 2010;5(12):e15306. https://doi.org/10.1371/journal.pone.0015306Venegas-Ortega MG, Flores-Gallegos AC, Martínez-Hernández JL, Aguilar CN, Nevárez-Moorillón GV. Production of Bioactive Peptides from Lactic Acid Bacteria: A Sustainable Approach for Healthier Foods. Compr Rev Food Sci Food Saf. 2019;18(4):1039-1051. doi: 10.1111/1541-4337.12455Venegas-Ortega MG, Flores-Gallegos AC, Martínez-Hernández JL, Aguilar CN, Nevárez-Moorillón G V. Production of Bioactive Peptides from Lactic Acid Bacteria: A Sustainable Approach for Healthier Foods. Compr Rev Food Sci Food Saf. 2019;18(4):1039-1051. doi: https://doi.org/10.1111/1541-4337.12455Iskandar CF, Cailliez-Grimal C, Borges F, Revol-Junelles AM. Review of lactose and galactose metabolism in Lactic Acid Bacteria dedicated to expert genomic annotation. Trends Food Sci Technol. 2019;88:121-132. doi: 10.1016/j.tifs.2019.03.020Iskandar CF, Cailliez-Grimal C, Borges F, Revol-Junelles AM. Review of lactose and galactose metabolism in Lactic Acid Bacteria dedicated to expert genomic annotation. Trends Food Sci Technol. 2019;88:121-132. doi: https://doi.org/10.1016/j.tifs.2019.03.020Garneau JE, Moineau S. Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb Cell Fact. 2011;10(S1):S20. doi: 10.1186/1475-2859-10-S1-S20Garneau JE, Moineau S. Bacteriophages of lactic acid bacteria and their impact on milk fermentations. Microb Cell Fact. 2011;10(1):S20. doi: 10.1186/1475-2859-10-S1-S20del Rio B, Binetti AG, Martín MC, Fernández M, Magadán AH, Alvarez MA. Multiplex PCR for the detection and identification of dairy bacteriophages in milk. Food Microbiol. 2007;24(1):75-81. doi: 10.1016/j.fm.2006.03.001del Rio B, Binetti AG, Martín MC, Fernández M, Magadán AH, Alvarez MA. Multiplex PCR for the detection and identification of dairy bacteriophages in milk. Food Microbiol. 2007;24(1):75-81. doi: https://doi.org/10.1016/j.fm.2006.03.001Gan R, Wu X, He W, et al. DNA phosphorothioate modifications influence the global transcriptional response and protect DNA from double-stranded breaks. Sci Rep. 2014;4:6642. doi: 10.1038/srep06642Gan R, Wu X, He W, et al. DNA phosphorothioate modifications influence the global transcriptional response and protect DNA from double-stranded breaks. Sci Rep. 2014;4(1):6642. doi: 10.1038/srep06642Ainsworth S, Sadovskaya I, Vinogradov E, et al. Differences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity. mBio. 2014;5(3):e00880-14. doi: 10.1128/mbio.00880-14Stuart A, Irina S, Evguenii V, et al. Differences in Lactococcal Cell Wall Polysaccharide Structure Are Major Determining Factors in Bacteriophage Sensitivity. mBio. 2014;5(3):10.1128/mbio.00880-14. doi: 10.1128/mbio.00880-14Chen J, Shen J, Ingvar Hellgren L, Ruhdal Jensen P, Solem C. Adaptation of Lactococcus lactis to high growth temperature leads to a dramatic increase in acidification rate. Sci Rep. 2015;5:14199. doi: 10.1038/srep14199Chen J, Shen J, Ingvar Hellgren L, Ruhdal Jensen P, Solem C. Adaptation of Lactococcus lactis to high growth temperature leads to a dramatic increase in acidification rate. Sci Rep. 2015;5(1):14199. doi: 10.1038/srep14199Martin MG, Magni C, de Mendoza D, López P. CitI, a Transcription Factor Involved in Regulation of Citrate Metabolism in Lactic Acid Bacteria. J Bacteriol. 2005;187(15):5146-5155. doi: 10.1128/jb.187.15.5146-5155.2005G MM, Christian M, Diego de M, Paloma L. CitI, a Transcription Factor Involved in Regulation of Citrate Metabolism in Lactic Acid Bacteria. J Bacteriol. 2005;187(15):5146-5155. doi: 10.1128/jb.187.15.5146-5155.2005Shi Z, Fan X, Tu M, Wu Z, Pan D. Comparison of changes in fermented milk quality due to differences in the proteolytic system between Lactobacillus helveticus R0052 and Lactococcus lactis subsp. lactis JCM5805. Food Biosci. 2023;51:102271. doi: 10.1016/j.fbio.2022.102271Shi Z, Fan X, Tu M, Wu Z, Pan D. Comparison of changes in fermented milk quality due to differences in the proteolytic system between Lactobacillus helveticus R0052 and Lactococcus lactis subsp. lactis JCM5805. Food Biosci. 2023;51:102271.Rodríguez J, Vázquez L, Flórez AB, Mayo B. Phenotype testing, genome analysis, and metabolic interactions of three lactic acid bacteria strains existing as a consortium in a naturally fermented milk. Front Microbiol. 2022;13:1000683. doi: 10.3389/fmicb.2022.1000683Rodríguez J, Vázquez L, Flórez AB, Mayo B. Phenotype testing, genome analysis, and metabolic interactions of three lactic acid bacteria strains existing as a consortium in a naturally fermented milk. Front Microbiol. 2022;Volume 13-2022. https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2022.1000683Chopin MC, Chopin A, Bidnenko E. Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol. 2005;8(4):473-479. doi: 10.1016/j.mib.2005.06.006Chopin MC, Chopin A, Bidnenko E. Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol. 2005;8(4):473-479. doi: https://doi.org/10.1016/j.mib.2005.06.006Jolicoeur AP, Lemay ML, Beaubien E, et al. Longitudinal Study of Lactococcus Phages in a Canadian Cheese Factory. Appl Environ Microbiol. 2023;89(5):e0042123. doi: 10.1128/aem.00421-23P JA, Marie-Laurence L, Elyse B, et al. Longitudinal Study of Lactococcus Phages in a Canadian Cheese Factory. Appl Environ Microbiol. 2023;89(5):e00421-23. doi: 10.1128/aem.00421-23Mileriene J, Aksomaitiene J, Kondrotiene K, et al. Whole-Genome Sequence of Lactococcus lactis Subsp. lactis LL16 Confirms Safety, Probiotic Potential, and Reveals Functional Traits. Microorganisms. 2023;11(4):1034. doi: 10.3390/microorganisms11041034Garvie EI, Farrow JAE. NOTES: Streptococcus lactis subsp. cremoris (Orla-Jensen) comb. nov. and Streptococcus lactis subsp. diacetilactis (Matuszewski et al.) nom. rev., comb. nov. Int J Syst Bacteriol. 1982;32(4):453-455. doi: 10.1099/00207713-32-4-453