Identification of Species and Subspecies of Lactic Acid Bacteria Present in Spanish Cheeses Type “Torta” by MALDI-TOF MS and pheS gene Analyses
Open accessAbstract
Several artisanal cheeses are elaborated in European countries, being commonly curdled with rennets of animal origin. However, in some Spanish regions some cheeses of type “Torta” are elaborated using Cynara cardunculus L. rennets. Two of these cheeses, “Torta del Casar” and “Torta de Trujillo”, are elaborated in Cáceres province with ewe’s raw milk and matured over at least 60 days without starters. In this work, we identified the lactic acid bacteria present in these cheeses using MALDI-TOF MS and pheS gene analyses, which showed they belong to the species Lactobacillus curvatus, Lactobacillus diolivorans, Lactobacillus paracasei, Lactobacillus plantarum, Lactobacillus rhamnosus, Lactococcus lactis and Leuconostoc mesenteroides. The pheS gene analysis also allowed the identification of the subspecies La. plantarum subsp. plantarum, La. paracasei subsp. paracasei and Le. mesenteroides subsp. jonggajibkimchii. Low similarity values were found in this gene for some currently accepted subspecies of Lc. lactis and for the two subspecies of La. plantarum, and values near to 100% for the subspecies of Le. mesenteroides and La. paracasei. These results, which were confirmed by the calculated ANIb and dDDH values of their whole genomes, showed the need to revise the taxonomic status of these species and their subspecies.
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Within the genus Leuconostoc, the species Ln. mesenteroides, Ln. peseudomesenteroides, and Ln. citreum have been detected in artisanal cheeses produced from raw milk.
“Within the genus Leuconostoc, the species Ln. mesenteroides, Ln. peseudomesenteroides, and Ln. citreum have been detected in artisanal cheeses produced from raw milk [122,123,124,125].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [124]
The Introduction states that Torta del Casar is made from ewe’s raw milk, and the Conclusions identify Leuconostoc mesenteroides in the two Torta cheeses studied (page numbers unavailable). The paper does not report detecting Ln. pseudomesenteroides or Ln. citreum, so it supports only one of the three species named. (LLM, conf=0.90)
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Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
The neighbor-joining method: a new method for reconstructing phylogenetic trees.
Saitou, N., & Nei, M. (1987) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a040454 · Cited by 59,962 · see citing works
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
Kumar, S., Stecher, G., & Tamura, K. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw054 · Cited by 43,923 · see citing works
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 39,119 · see citing works
Kimura, M. (1980) · Journal of Molecular Evolution · doi:10.1007/bf01731581 · Cited by 29,778 · see citing works
Genome sequence-based species delimitation with confidence intervals and improved distance functions
Meier‐Kolthoff, J. P., Auch, A. F., Klenk, H., & Göker, M. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-60 · Cited by 6,761 · see citing works
Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes
Chun, J., Oren, A., Ventosa, A., Christensen, H. K., Arahal, D. R., da Costa, M. S., Rooney, A. P., Yi, H., Xu, X.-W., Meyer, S. E. D., et al. (2018) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijsem.0.002516 · Cited by 3,100 · see citing works
JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison
Richter, M., Rossello-Mora, R. A., Glöckner, F. O., & Peplies, J. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv681 · Cited by 2,920 · see citing works
Auch, A. F., von Jan, M., Klenk, H., & Göker, M. (2010) · Standards in Genomic Sciences · doi:10.4056/sigs.531120 · Cited by 1,757 · see citing works
Meier‐Kolthoff, J. P., Hahnke, R. L., Petersen, J., Scheuner, C., Michael, V., Fiebig, A., Rohde, C., Rohde, M., Fartmann, B., Goodwin, L., et al. (2014) · Standards in Genomic Sciences · doi:10.1186/1944-3277-9-2 · Cited by 617 · see citing works
Food-Origin Lactic Acid Bacteria May Exhibit Probiotic Properties: Review
Zielińska, D., & Kołożyn‐Krajewska, D. (2018) · BioMed Research International · doi:10.1155/2018/5063185 · Cited by 212 · see citing works
Domingos-Lopes, M. F. P., Stanton, C., Ross, P. R., Dapkevicius, M. L. E., & Silva, C. C. G. (2017) · Food Microbiology · doi:10.1016/j.fm.2016.11.014 · Cited by 210 · see citing works
Nacef, M., Chevalier, M., Chollet, S., Drider, D., & Flahaut, C. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.07.005 · Cited by 131 · see citing works
Nguyen, D. T. L., Hoorde, K. V., Cnockaert, M. C., Brandt, E. D., Aerts, M., Thanh, L. B., & Vandamme, P. A. R. (2013) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2013.01.024 · Cited by 130 · see citing works
Ferreira, L., Sánchez‐Juanes, F., García‐Fraile, P., Rivas, R., Mateos, P. F., Martı́nez-Molina, E., González‐Buitrago, J. M., & Velázquez, E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020223 · Cited by 110 · see citing works
Self-citationMicrobial diversity and dynamics during the production of May bryndza cheese
Pangallo, D., Šaková, N., Koreňová, J., Puškárová, A., Kraková, L., Valík, Ľ., & Kuchta, T. (2013) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2013.10.015 · Cited by 102 · see citing works
Franciosi, E., Carafa, I., Nardin, T., Schiavon, S., Poznanski, E., Cavazza, A., Larcher, R., & Tuohy, K. M. (2015) · BioMed Research International · doi:10.1155/2015/625740 · Cited by 94 · see citing works
Doan, N. T. L., Hoorde, K. V., Cnockaert, M. C., Brandt, E. D., Aerts, M., Thanh, B. L., & Vandamme, P. A. R. (2012) · Letters in Applied Microbiology · doi:10.1111/j.1472-765x.2012.03287.x · Cited by 78 · see citing works
Tanigawa, K., Kawabata, H., & Watanabe, K. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.02698-09 · Cited by 77 · see citing works
(2016) · Wiley eBooks · doi:10.1002/9783527807796 · Cited by 71 · see citing works
Pogačić, T., Mancini, A., Santarelli, M., Bottari, B., Lazzi, C., Neviani, E., & Gatti, M. (2013) · Food Microbiology · doi:10.1016/j.fm.2013.05.009 · Cited by 70 · see citing works
Foschi, C., Laghi, L., Parolin, C., Giordani, B., Compri, M., Cevenini, R., Marangoni, A., & Vitali, B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172483 · Cited by 58 · see citing works
Main lactic acid bacteria isolated during ripening of Casar de Cáceres cheese
Poullet, B., Huertas, M., Sánchez, A., Cáceres, P., & Larriba, G. (1993) · Journal of Dairy Research · doi:10.1017/s0022029900027412 · Cited by 47 · see citing works
Ordiales, E., Benito, M. J., Martı́n, A., Casquete, R., Serradilla, M. J., & Córdoba, M. D. G. (2013) · Food Control · doi:10.1016/j.foodcont.2013.03.027 · Cited by 40 · see citing works
Sato, H., Torimura, M., Kitahara, M., Ohkuma, M., Hotta, Y., & Tamura, H. (2012) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2012.08.008 · Cited by 39 · see citing works
Morandi, S., Brasca, M., & Lodi, R. (2011) · Dairy Science and Technology · doi:10.1007/s13594-011-0016-7 · Cited by 35 · see citing works
Colombo, E. V., Franzetti, L., FRUSCA, M., & Scarpellini, M. (2010) · Journal of Food Protection · doi:10.4315/0362-028x-73.4.657 · Cited by 31 · see citing works
Rodríguez, L. G. R., Bleckwedel, J., Ortiz, M. E., Pescuma, M., & Mozzi, F. (2016) · Industrial Biotechnology · doi:10.1002/9783527807796.ch11 · Cited by 29 · see citing works
Yao, A. A., Schümann, P., Thonart, P., Djè, K. M., & Pukall, R. (2014) · The Open Microbiology Journal · doi:10.2174/1874285801408010078 · Cited by 19 · see citing works
Ludwig, W., Schleifer, K., & Whitman, W. B. (2015) · Bergey's Manual of Systematics of Archaea and Bacteria · doi:10.1002/9781118960608.obm00058 · Cited by 13 · see citing works
Doijad, S. P., & Chakraborty, T. (2019) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijsem.0.003706 · Cited by 7 · see citing works
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Grujović, M. Ž., Mladenović, K., Semedo‐Lemsaddek, T., Laranjo, M., Stefanović, O. D., & Kocić‐Tanackov, S. (2022) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12897 · Cited by 161 · see citing works
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Self-citationBosco, F., Cirrincione, S., Carletto, R. A., Marmo, L., Chiesa, F., Mazzoli, R., & Pessione, E. (2021) · Microorganisms · doi:10.3390/microorganisms9122426 · Cited by 39 · see citing works
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Yu, K., Huang, Z., Li, Y., Fu, Q., Lin, L., Wu, S., Dai, H., Cai, H., Xiao, Y., Lan, R., et al. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.625821 · Cited by 27 · see citing works
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Abarquero, D., Renes, E., Combarros‐Fuertes, P., Fresno, J. M., & Tornadijo, M. E. (2022) · LWT · doi:10.1016/j.lwt.2022.114121 · Cited by 27 · see citing works
Tabla, R., & Roa, I. (2022) · LWT · doi:10.1016/j.lwt.2022.114066 · Cited by 23 · see citing works
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Self-citation
- Authors
- Sánchez-Juanes, F., Teixeira-Martín, V., González-Buitrago, J. M., Velázquez, E., & Flores-Félix, J. D.
- Affiliations
- Instituto de Investigación Biomédica de Salamanca (IBSAL), Complejo Asistencial Universitario de Salamanca, Universidad de Salamanca, CSIC, 37007 Salamanca, Spain
- Universidad de Salamanca (ES)
- Departamento de Microbiología y Genética and Instituto Hispanoluso de Investigaciones Agrarias (CIALE), Universidad de Salamanca, Edificio Departamental de Biología, Lab 209. Av. Doctores de la Reina S/N, 37007 Salamanca, Spain
- Corresponding author
- Velázquez, Encarna
- Venue
- Microorganisms
- Publisher
- MDPI AG
- Published
- 2020-02-21
- Volume
- 8
- Issue
- 2
- Pages
- 301
- ISSN
- 2076-2607 (ISSN-L)
- PMC
- PMC7074959
- OpenAlex
- W3008338082
- Cited by
- 38
- References
- 31
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 4 · 2023: 4 · 2022: 10 · 2021: 7 · 2020: 5
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Microorganisms (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Gredos (University of Salamanca) (publishedVersion, cc-by-nc-nd)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Hispana (submittedVersion, cc-by-nc-nd)
- Funders
- Junta de Castilla y León (CLU-2O18-04)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Clinical Biochemistry › Bacterial Identification and Susceptibility Testing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Identification and Quantification in Food
- Keywords
- lactic acid bacteria, Lactobacillus plantarum, Lactobacillus paracasei, Lactococcus lactis, Leuconostoc mesenteroides, MALDI-TOF mass spectrometry, subspecies identification, ANIb, digital DNA-DNA hybridization, cheese microbiota, artisanal cheese
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