The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.
Functional implications of the microbial community structure of undefined mesophilic starter cultures
Open accessAbstract
This review describes the recent advances made in the studies of the microbial community of complex and undefined cheese starter cultures. We report on work related to the composition of the cultures at the level of genetic lineages, on the presence and activity of bacteriophages and on the population dynamics during cheese making and during starter culture propagation. Furthermore, the link between starter composition and starter functionality will be discussed. Finally, recent advances in predictive metabolic modelling of the multi-strain cultures will be discussed in the context of microbe-microbe interactions.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Because Leuconostoc are obligate heterofermenters, production of CO2 may alter texture and cause late blowing in certain cheeses, although this often leads to moderate "eye" formation in cheese.
“Because they are obligate heterofermenters, the production of CO2 may alter texture and cause late blowing in certain cheeses, although this often leads to moderate “eye” formation in cheese [88,95].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [95]
In “Population dynamics during cheese making” (page not provided), the paper says heterofermentative Leuconostoc mesenteroides produces CO2 that leads to moderate eye formation in cheese. It does not say that this gas causes late blowing or otherwise alters texture in certain cheeses, nor does it explicitly describe Leuconostoc as obligate heterofermenters. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn artisanal raw milk cheeses, spontaneous fermentation is driven by the development of the aforementioned microbiota, but the outcome is unpredictable because the physiological stage and extent of inoculum are beyond operator control.
“In these cheeses, the spontaneous fermentation of the milk is driven by the development of the aforementioned microbiota. However, the outcome of such processes is unpredictable, as the physiological stage and extent of inoculum are beyond operator’s control [95].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [95]
The Introduction section “Composition of undefined complex cheese starters” (page unavailable) says spontaneous fermentation is driven by microbiota in the raw material and that its outcome is unpredictable because the material determines the inoculum’s composition and microbial load. This supports the claim about unpredictable outcomes and inoculum extent, but the passage does not identify the inoculum’s physiological stage as a reason. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe cultures used for the production of Gouda cheese were isolated from an undefined starter culture traditionally used for the production of this cheese, consisting of L. lactis subsp. cremoris, L. lactis subsp. lactis biovar diacetylactis, and Ln. mesenteroides.
“For instance, the cultures used for the production of Gouda cheese were isolated from an undefined starter culture traditionally used for the production of this cheese, consisting of L. lactis subsp. cremoris, L. lactis subsp. lactis biovar diacetylactis, and Ln. mesenteroides [95,112].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [95]
Defined starter cultures usually consist of one or more strains with known characteristics.
“The former usually consist of one or more strains with known characteristics [95].”
From Lactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions (2022) · cites this paper as [95]
The whey left after manufacturing has a unique temperature, chemical composition, and microflora, varying by species and biotypes depending on the chosen technology and type of milk.
“The whey left after manufacturing has a unique temperature, chemical composition, and microflora, varying by species and biotypes depending on the chosen technology and type of milk [21,59,73,76,80,109,110,111,112].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [111]
The Introduction sections on starter-culture composition and population dynamics discuss microbes in milk and cheese, not the whey left after manufacturing. Searches for whey, its temperature and chemical composition, and variation by milk type or manufacturing technology found no passage addressing those claims. The indexed passages provide no page numbers. (LLM, conf=0.75)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
A medium for the cultivation of lactobacilli
De MAN, J. C., ROGOSA, M., & SHARPE, M. E. (1960) · Journal of Applied Bacteriology · doi:10.1111/j.1365-2672.1960.tb00188.x · Cited by 5,311
Lactic acid bacteria as functional starter cultures for the food fermentation industry
Leroy, F., & De Vuyst, L. (2004) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2003.09.004 · Cited by 1,852
Biochemical pathways for the production of flavour compounds in cheeses during ripening: A review
McSweeney, P. L. H., & Sousa, M. J. (2000) · Le Lait · doi:10.1051/lait:2000127 · Cited by 1,266 · cited 1×
“mesenteroides can only produce diacetyl and acetoin from citrate at acidic pH [42] and acidification is predominantly driven by lactose fermentation by the lactococci [41].”
BackgroundThingstad, T. F. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.6.1320 · Cited by 1,085
Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products
Smit, G., Smit, B. A., & Engels, W. J. M. (2005) · FEMS Microbiology Reviews · doi:10.1016/j.fmrre.2005.04.002 · Cited by 949
Explaining Microbial Population Genomics through Phage Predation
Rodriguez-Valera, F., Martin-Cuadrado, A.-B., Rodriguez-Brito, B., Pašić, L., Thingstad, T. F., Rohwer, F., & Mira, A. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2235 · Cited by 663
Use of Propidium Monoazide for Live/Dead Distinction in Microbial Ecology
Nocker, A., Sossa-Fernandez, P., Burr, M. D., & Camper, A. K. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.02987-06 · Cited by 580
A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid
Cotter, P. D., Gahan, C. G. M., & Hill, C. (2001) · Molecular Microbiology · doi:10.1046/j.1365-2958.2001.02398.x · Cited by 385
Production of Aroma Compounds in Lactic Fermentations
Smid, E. J., & Kleerebezem, M. (2014) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030713-092339 · Cited by 366
Self-citationMicrobe-Microbe Interactions in Mixed Culture Food Fermentations
Smid, E. J., & Lacroix, C. (2013) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2012.11.007 · Cited by 348
Self-citationFermented foods and food safety
Nout, M. J. R. (1994) · Food Research International · doi:10.1016/0963-9969(94)90097-3 · Cited by 324
Leuconostoc, characteristics, use in dairy technology and prospects in functional foods
Hemme, D., & Foucaud-Scheunemann, C. (2004) · International Dairy Journal · doi:10.1016/j.idairyj.2003.10.005 · Cited by 323
Teusink, B., Wiersma, A., Molenaar, D., Francke, C., de Vos, W. M., Siezen, R. J., & Smid, E. J. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606263200 · Cited by 284
Self-citationMultifactorial Diversity Sustains Microbial Community Stability
Erkus, O., de Jager, V. C. L., Spus, M., van Alen-Boerrigter, I. J., van Rijswijck, I. M. H., Hazelwood, L., Janssen, P. W. M., van Hijum, S. A. F. T., Kleerebezem, M., & Smid, E. J. (2013) · The ISME Journal · doi:10.1038/ismej.2013.108 · Cited by 217
Self-citationProteolytic systems in lactic acid bacteria
Law, B. A., & Kolstad, J. (1983) · Antonie van Leeuwenhoek · doi:10.1007/bf00399500 · Cited by 210
Interactions between non-starter microorganisms during cheese manufacture and repening
Martley, F. G., & Crow, V. L. (1993) · International Dairy Journal · doi:10.1016/0958-6946(93)90027-w · Cited by 189
The Lactococcus lactis CodY Regulon
den Hengst, C. D., van Hijum, S. A. F. T., Geurts, J. M. W., Nauta, A., Kok, J., & Kuipers, O. P. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502349200 · Cited by 189
Modelling strategies for the industrial exploitation of lactic acid bacteria
Teusink, B., & Smid, E. J. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1319 · Cited by 157
Self-citationGuédon, É., Sperandio, B., Pons, N., Ehrlich, S. D., & Renault, P. (2005) · Microbiology · doi:10.1099/mic.0.28186-0 · Cited by 142
Metabolism of Leuconostoc Bacteria
Cogan, T. M., & JORDAN, K. N. (1994) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(94)77213-1 · Cited by 125
Broadbent, J. R., Cai, H., Larsen, R. L., Hughes, J. E., Welker, D. L., De Carvalho, V. G., Tompkins, T. A., Ardö, Y., Vogensen, F., De Lorentiis, A., et al. (2011) · Journal of Dairy Science · doi:10.3168/jds.2010-4068 · Cited by 124 · cited 1×
“Peptide degradation by released peptides plays a role in debittering of the ripening cheese, thereby affecting primarily the taste of the product [30].”
BackgroundCollins, Y. F., McSweeney, P. L. H., & Wilkinson, M. G. (2003) · Journal of Dairy Research · doi:10.1017/s0022029902005915 · Cited by 119
Rademaker, J. L. W., Herbet, H., Starrenburg, M. J. C., Naser, S. M., Gevers, D., Kelly, W. J., Hugenholtz, J., Swings, J., & Vlieg, J. E. T. V. H. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01017-07 · Cited by 111
Schoustra, S. E., Kasase, C., Toarta, C., Kassen, R., & Poulain, A. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063948 · Cited by 110
The cell membrane and the struggle for life of lactic acid bacteria
Konings, W. N. (2002) · Springer eBooks · doi:10.1007/978-94-017-2029-8_2 · Cited by 110
The cell membrane and the struggle for life of lactic acid bacteria
Konings, W. N. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020604203977 · Cited by 102
García-Quintáns, N., Magni, C., de Mendoza, D., & López, P. (1998) · Applied and Environmental Microbiology · doi:10.1128/aem.64.3.850-857.1998 · Cited by 88
Novel characteristic for distinguishing Lactococcus lactis subsp. lactis from subsp. cremoris
Nomura, M., Kimoto, H., Someya, Y., & Suzuki, I. (1999) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/00207713-49-1-163 · Cited by 83
A review of the molecular approaches to investigate the diversity and activity of cheese microbiota
Ndoye, B., Rasolofo, E. A., LaPointe, G., & Roy, D. (2011) · Dairy Science and Technology · doi:10.1007/s13594-011-0031-8 · Cited by 78
Hugenholtz, J., Perdon, L., & Abee, T. (1993) · Applied and Environmental Microbiology · doi:10.1128/aem.59.12.4216-4222.1993 · Cited by 70
Lactic acid bacteria in the dairy industry
Sharpe, M. E. (1979) · International Journal of Dairy Technology · doi:10.1111/j.1471-0307.1979.tb01402.x · Cited by 69
How does Listeria monocytogenes combat acid conditions?
Smith, J. L., Liu, Y., & Paoli, G. C. (2012) · Canadian Journal of Microbiology · doi:10.1139/cjm-2012-0392 · Cited by 64
Erkuş, O., de Jager, V. C. L., Geene Renske, T. C. M., van Alen-Boerrigter, I., Hazelwood, L. A., van Hijum, S. A. F. T., Kleerebezem, M., & Smid, E. J. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.03.027 · Cited by 64
Self-citationHigh local substrate availability stabilizes a cooperative trait
Bachmann, H., Douwe Molenaar, B., Kleerebezem, M., & Vlieg, J. E. T. V. H. (2010) · The ISME Journal · doi:10.1038/ismej.2010.179 · Cited by 58
Self-citationA high-throughput cheese manufacturing model for effective cheese starter culture screening
Bachmann, H., Kruijswijk, Z., Douwe Molenaar, B., Kleerebezem, M., & Vlieg, J. E. T. V. H. (2009) · Journal of Dairy Science · doi:10.3168/jds.2009-2372 · Cited by 58
Self-citationSelection of Protease-Positive and Protease-Negative Variants of Streptococcus cremoris
Hugenholtz, J., Splint, R., Konings, W. N., & Veldkamp, H. (1987) · Applied and Environmental Microbiology · doi:10.1128/aem.53.2.309-314.1987 · Cited by 52
Differentiation of lactococci by rRNA gene restriction analysis
Köhler, G., Ludwig, W., & Schleifer, K. H. (1991) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1991.tb04615.x · Cited by 43
Agar Medium for Differential Enumeration of Lactic Streptococci
Reddy, M. S., Vedamuthu, E. R., Washam, C. J., & Reinbold, G. W. (1972) · Applied Microbiology · doi:10.1128/am.24.6.947-952.1972 · Cited by 42
Metabolic models for rational improvement of lactic acid bacteria as cell factories
Smid, E. J., Enckevort, F. J. H., Wegkamp, A., Boekhorst, J., Molenaar, D., Hugenholtz, J., Siezen, R. J., & Teusink, B. (2005) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2005.02652.x · Cited by 38
Self-citationFunctional ingredient production: application of global metabolic models
Smid, E. J., Molenaar, D., Hugenholtz, J., de Vos, W. M., & Teusink, B. (2005) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2005.03.001 · Cited by 36
Self-citationDesfossés-Foucault, É., LaPointe, G., & Roy, D. (2014) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2014.03.004 · Cited by 35
Time‐resolved genetic responses of Lactococcus lactis to a dairy environment
Bachmann, H., de Wilt, L. H. A. M., Kleerebezem, M., & Vlieg, J. E. T. V. H. (2010) · Environmental Microbiology · doi:10.1111/j.1462-2920.2010.02168.x · Cited by 34
Self-citationThe Secreted Esterase of Propionibacterium freudenreichii Has a Major Role in Cheese Lipolysis
Mukdsi, M. C. A., Falentin, H., Maillard, M.-B., et al. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.03640-13 · Cited by 32
Brandsma, J. B., van de Kraats, I., Abee, T., Zwietering, M. H., & Meijer, W. C. (2011) · Food Microbiology · doi:10.1016/j.fm.2011.08.012 · Cited by 32
Replication Regions of Two Pairs of Incompatible Lactococcal Theta-Replicating Plasmids
Gravesen, A., von Wright, A., Josephsen, J., et al. (1997) · Plasmid · doi:10.1006/plas.1997.1302 · Cited by 25
Kutahya, O., Starrenburg, M. J. C., Rademaker, J. L. W., Klaassen, C. H. W., Vlieg, J. E. T. V. H., Smid, E. J., & Kleerebezem, M. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.00518-11 · Cited by 23
Self-citationGibert, I., & Barbé, J. (1990) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1990.tb13956.x · Cited by 20
Winkel, S. A., & Richardson, G. H. (1984) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(84)81646-x · Cited by 15
Barrette, J., Champagne, C. P., Roy, D., & Rodrigue, N. (2000) · Journal of Industrial Microbiology & Biotechnology · doi:10.1038/sj.jim.7000105 · Cited by 12
Erkuş, O. (2014) · doi:10.18174/305064 · Cited by 4
Flagged first, then by citations
Cited by
Sorted by citations
Stress Physiology of Lactic Acid Bacteria.
Papadimitriou, K., Alegría, Á., Bron, P. A., de Angelis, M., Gobbetti, M., Kleerebezem, M., Lemos, J. A., Linares, D. M., Ross, P., Stanton, C., et al. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00076-15 · Cited by 914
Self-citationLactic Acid Bacteria in Raw-Milk Cheeses: From Starter Cultures to Probiotic Functions
Coelho, M. C., Malcata, F. X., & Silva, C. C. G. (2022) · Foods · doi:10.3390/foods11152276 · Cited by 276
“Because they are obligate heterofermenters, the production of CO2 may alter texture and cause late blowing in certain cheeses, although this often leads to moderate “eye” formation in cheese [88,95].”
BackgroundMetabolic network modeling of microbial communities
Biggs, M. B., Medlock, G. L., Kolling, G. L., & Papin, J. A. (2015) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1308 · Cited by 124
Functional Strain Redundancy and Persistent Phage Infection in Swiss Hard Cheese Starter Cultures
Somerville, V., Berthoud, H., Schmidt, R. S., Bachmann, H.-P., Meng, Y. H., Fuchsmann, P., von Ah, U., & Engel, P. (2022) · The ISME Journal · doi:10.1038/s41396-021-01071-0 · Cited by 55
Next-generation sequencing as an approach to dairy starter selection
Kelleher, P., Murphy, J., Mahony, J., & van Sinderen, D. (2015) · Dairy Science & Technology · doi:10.1007/s13594-015-0227-4 · Cited by 51
Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking
Neviani, E., Gatti, M., Gardini, F., & Levante, A. (2025) · Foods · doi:10.3390/foods14050830 · Cited by 44
Microbial characterization of an artisanal production of Robiola di Roccaverano cheese
Biolcati, F., Andrighetto, C., Bottero, M. T., & Dalmasso, A. (2020) · Journal of Dairy Science · doi:10.3168/jds.2019-17451 · Cited by 26
Biolcati, F., Ferrocino, I., Bottero, M. T., & Dalmasso, A. (2020) · Journal of Dairy Science · doi:10.3168/jds.2020-18208 · Cited by 20
Metadata
- Authors
- Smid, E. J., Erkus, O., Spus, M., Wolkers-Rooijackers, J. C., Alexeeva, S., & Kleerebezem, M.
- Affiliations
- TiFN (NL)
- Corresponding author
- Smid, Eddy J
- Venue
- Microbial Cell Factories
- Published
- 2014
- Volume
- 13
- Issue
- Suppl 1
- Pages
- S2
- ISSN
- 1475-2859 (ISSN-L)
- PMC
- PMC4155819
- OpenAlex
- W2155911451
- Cited by
- 117
- References
- 50
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 10 · 2023: 7 · 2022: 11 · 2021: 8 · 2020: 11 · 2019: 12 · 2018: 10 · 2017: 13 · 2016: 11 · 2015: 11
- Type
- conference abstract
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Microbial Cell Factories (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
- Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
- Keywords
- cheese starter cultures, microbial community structure, mesophilic lactic acid bacteria, bacteriophages, population dynamics, cheese production, microbial interactions
- MeSH terms
- Cheese, Fermentation, Food Microbiology, Genetic Linkage, Lactococcus lactis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
