How the fewest become the greatest. L. casei’ s impact on long ripened cheeses.
Open accessAbstract
Lactobacillus casei group, including species classified currently as L. casei, L. paracasei, and L. rhamnosus, are among the most frequently found species in raw milk, hard cooked, long-ripened cheeses. Starting from very low amounts in raw milk, they become dominant in the cheese during ripening, selected by several technological drivers. Their presence at different stages of cheese making and ripening turned out to be crucial to define cheese features. For these reasons, the scientific community has been more and more busy in studying this “tiny but mighty microbes” and their effect in cheeses. The present paper aims to review the current literature on this topic, with particular reference to the case of Parmigiano Reggiano and Grana Padano, two of the most famous PDO Italian cheeses. Recent advances regarding the possibility to select new wild strains capable to persist to the end of ripening, carrying out a slow but crucial activity and with specific aromatic features, are also presented.
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The enzymes produced by LAB communities in raw milk support proteolysis and lipolysis, which are chief drivers of flavor and texture of cheese.
“During cheese ripening, proteolysis is of great importance because it contributes to textural and sensory changes in the matrix of this product [30].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [31]
In the Introduction’s “What’s Their Effect?” section, the paper identifies proteolysis as a major pathway in flavor formation during cheese ripening, supporting the citing sentence’s sensory-change point. It does not say that proteolysis causes textural changes; its “Who Are They?” section instead links curd texture to cooking and starter-LAB acidity. (LLM, conf=0.84)
Experimental — accuracy not yet measuredFree amino acids from proteolysis and fatty acids from lipolysis act as substrates for secondary reactions that produce important flavor compounds.
“The free amino acids resulting from proteolysis and the fatty acids released by lipolysis play an active role as substrates for a number of secondary reactions, which give rise to many important flavor compounds [31,32,33].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [31]
After the brining step (1-month-old samples and later), a compositional change occurs in cheese microbiota that shows a decrease in the relative abundance of SLAB species, while NSLAB population, initially present at low abundances, find suitable conditions for development.
“After the brining step (1-month-old samples and later), a compositional change occurs in cheese microbiota that shows a decrease in the relative abundance of the SLAB species, while NSLAB population, initially present at low abundances, find suitable conditions for development (Lazzi et al., 2014; Bottari et al., 2018).”
From The Interrelationship Between Microbiota and Peptides During Ripening as a Driver for Parmigiano Reggiano Cheese Quality (2020) · cites this paper as Bottari et al., 2018
Major differences among dairies between 1 and 2 months old samples and 7 and 9 months old samples are consistent with the growth of NSLAB coming mainly from raw milk and their higher adaptability to specific environmental conditions, driven by cheese making parameters.
“Major differences revealed among dairies between 1 and 2 months old samples and 7 and 9 months old samples, are consistent with the growth of NSLAB coming mainly from raw milk and their higher adaptability to specific environmental conditions, driven by cheese making parameters (Bottari et al., 2018).”
From The Interrelationship Between Microbiota and Peptides During Ripening as a Driver for Parmigiano Reggiano Cheese Quality (2020) · cites this paper as Bottari et al., 2018
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“…from raw cow’s milk, where they are not the prevalent genus [6] but possess adaptation capabilities that allow them to survive the initial steps of the manufacturing process, making Lb. casei group the dominant microbiota of raw milk hard cheeses during the subsequent ripening process [7,8].”
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“L. rhamnosus, L. casei and L. paracasei are in fact NSLAB species well known for their capability to better adapt and grow during even prolonged ripening periods (Bottari et al., 2018; Lazzi et al., 2016).”
Martini, S., Solà, L., Cattivelli, A., Cristofolini, M., Pizzamiglio, V., Tagliazucchi, D., & Solieri, L. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1342180 · Cited by 11 · see citing works
“These mesophilic and facultatively heterofermentative species belong to the so-called Lcb. casei group (LCG) and are supposed to arise from raw cow milk and dairy environment (Bottari et al., 2018).”
BackgroundInfluentialMinervini, F., & Calasso, M. P. (2015) · Encyclopedia of Dairy Sciences · doi:10.1016/b978-0-08-100596-5.00853-2 · Cited by 10 · see citing works
Loffi, C., Bortolazzo, E., Garavaldi, A., Musi, V., Reverberi, P., Galaverna, G., Sforza, S., & Tedeschi, T. (2021) · Foods · doi:10.3390/foods10040770 · Cited by 9 · see citing works
“Parmigiano Reggiano is then subjected to at least 12 months of ripening, in which, among other processes, starter lactic acid bacteria are progressively replaced by non-starter ones [3].”
BackgroundValentino, V., Magliulo, R., Balivo, A., Krysmann, A., Calvanese, C. M., Esposito, A., Sequino, G., Genovese, A., Porcellato, D., Ercolini, D., et al. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00815-6 · Cited by 8 · see citing works
“The proteolytic and lipolytic potential of these microorganisms favor their adaptation during the cheese ripening, when lactose is exhausted, thus explaining their dominancein long-ripened cheeses 7,13,22 .”
Rossi, A., Marroni, F., Renoldi, N., Filippo, G. D., Gover, E., Marino, M., & Innocente, N. (2024) · Journal of Dairy Science · doi:10.3168/jds.2024-24463 · Cited by 6 · see citing works
Screening of Aroma-Producing Performance of Anticlostridial Lacticaseibacillus casei Strains
Renoldi, N., Innocente, N., Rossi, A., Brasca, M., Morandi, S., & Marino, M. (2024) · Food and Bioprocess Technology · doi:10.1007/s11947-023-03311-x · Cited by 6 · see citing works
“…Lb. rhamnosus, is of great relevance since all these species have been frequently found in different semi-hard and hard cheeses at late stages of ripening, suggesting the a�nity of these microorganisms to the NSLAB (Non Starter Lactic Acid Bacteria) group (Bottari et al. 2018; Gatti et al. 2014).”
Sousa, R. J. M., Ribeiro, S. C., Baptista, J., & Silva, C. C. G. (2023) · Journal of Dairy Research · doi:10.1017/s0022029923000043 · Cited by 5 · see citing works
“Cheese made from raw milk has a high bacterial diversity that is not destroyed by pasteurization (Bottari et al., 2018).”
BackgroundProvolone del Monaco PDO cheese: Lactic microflora, biogenic amines and volatilome characterization
Scarano, L., Peruzy, M. F., Fallico, V., Blaiotta, G., Aponte, M., Anastasio, A., & Murru, N. (2024) · Food Research International · doi:10.1016/j.foodres.2024.115257 · Cited by 3 · see citing works
Metataxonomic analysis of bacterial and fungal communities in colonial cheese
Myazaki, N. L., Cardoso, M., & Verruck, S. (2024) · Food Science and Technology · doi:10.5327/fst.00153 · Cited by 3 · see citing works
Salt in Cheese: Physical, Chemical, Biological, and Sensory Aspects—Water Activity
Bisig, W., Arias‐Roth, E., Fröhlich‐Wyder, M., Guggisberg, D., Jakob, E., Sheehan, J. J., & Skeie, S. B. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-15956-5.00020-8 · Cited by 2 · see citing works
Arthrospira platensis Extract: A Non-Invasive Strategy to Obtain Adjunct Attenuated Cultures
Bancalari, E., Martelli, F., Bottari, B., Neviani, E., & Gatti, M. (2021) · Foods · doi:10.3390/foods10030588 · Cited by 2 · see citing works
Künz, J. J., Roch, F., Dzieciol, M., Sofka, D., Hilbert, F., & Selberherr, E. (2025) · Frontiers in Microbiology · doi:10.3389/fmicb.2025.1617995 · Cited by 1 · see citing works
Characterization of Tiroler Bergkäse PDO cheese: A multimethodological approach
Innerbichler, H., Trockenbacher, A., Höller, A., Scholl‐Bürgi, S., Vecchio, L. D., Cirlini, M., König, J. S., & Bach, K. E. (2025) · Food Chemistry Molecular Sciences · doi:10.1016/j.fochms.2025.100336 · Cited by 1 · see citing works
“Raw milk is the primary source of L. casei group members (Bottari, Levante, Neviani, & Gatti, 2018).”
Camelo‐Silva, C., Verruck, S., Luccio, M. D., Pimentel, T. C., Silva, M. C., Esmerino, E. A., & da Cruz, A. G. (2023) · doi:10.1002/9781119776406.ch4 · Cited by 1 · see citing works
Studio dell’attività di Lacticaseibacillus casei come agente antigonfiore in formaggi a latte crudo
Filippo, G. D., Marino, M., Brasca, M., Maifreni, M., & Innocente, N. (2022) · Scienza e Tecnica Lattiero Casearia · doi:10.36138/stlc.04.2022.03
Gatti, M., Bettera, L., Levante, A., Bancalari, E., Bottari, B., & Neviani, E. (2022) · Scienza e Tecnica Lattiero Casearia · doi:10.36138/stlc.05.2022.01
Renoldi, N., Innocente, N., Rossi, A., Brasca, M., Morandi, S., & Marino, M. (2023) · Research Square · doi:10.21203/rs.3.rs-3573518/v1
Secondary and Adjunct Cultures
Irlinger, F., Hélinck, S., & Jany, J. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-15956-5.00044-0
Bosnea, L. A., Kosma, I. S., Kakouri, A., Paramithiotis, S., & Samelis, J. (2025) · Fermentation · doi:10.3390/fermentation11120673
Bettera, L., Buzzanca, D., Levante, A., Cirlini, M., Saadoun, J. H., Martinengo, N., Chiarini, E., Faccia, M., Zeppa, G., Calasso, M. P., et al. (2026) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2026.111881
“This is consistent with evidence that non-starter LAB contribute to aroma formation during ripening of long ripened raw-milk cheeses (Bottari et al., 2018).”
Levante, A., Bettera, L., Bertani, G., Bancalari, E., Saadoun, J. H., Neviani, E., & Gatti, M. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.7459903
Alinovi, M., Prandi, B., Cirlini, M., Agulló, V., Monica, S., Calcinai, L., Parenti, O., Vecchio, L. D., Bresciani, L., Mena, P. R., et al. (2026) · Food Chemistry · doi:10.1016/j.foodchem.2026.151557
- Authors
- Bottari, B., Levante, A., Neviani, E., & Gatti, M.
- Affiliations
- University of Parma (IT)
- Corresponding author
- Bottari, Benedetta
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2018-11-22
- Volume
- 9
- Pages
- 2866-2866
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC6262004
- OpenAlex
- W2901932650
- Cited by
- 45
- References
- 66
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 6 · 2023: 11 · 2022: 4 · 2021: 6 · 2020: 5 · 2019: 3 · 2015: 1
- FWCI
- 0.35
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
- Life Sciences › Agricultural and Biological Sciences › Food Science › Advanced Scientific Research Methods
- Keywords
- Lactobacillus casei, Lactobacillus paracasei, Lactobacillus rhamnosus, Parmigiano Reggiano, Grana Padano, cheese ripening, cheese production, cheese aroma, lactic acid bacteria
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