Multifactorial Diversity Sustains Microbial Community Stability
Open accessAbstract
Maintenance of a high degree of biodiversity in homogeneous environments is poorly understood. A complex cheese starter culture with a long history of use was characterized as a model system to study simple microbial communities. Eight distinct genetic lineages were identified, encompassing two species: Lactococcus lactis and Leuconostoc mesenteroides. The genetic lineages were found to be collections of strains with variable plasmid content and phage sensitivities. Kill-the-winner hypothesis explaining the suppression of the fittest strains by density-dependent phage predation was operational at the strain level. This prevents the eradication of entire genetic lineages from the community during propagation regimes (back-slopping), stabilizing the genetic heterogeneity in the starter culture against environmental uncertainty.
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This resistance can be attributed to the presence of bacteriophages within complex starter cultures, where they drive the generation of genetic and phenotypic diversity.
“This phenomenon can be attributed to the presence of bacteriophages within complex starter cultures, where they play an essential role as part of the microbial community, driving the generation of genetic and phenotypic diversity in the microbial population [27,28].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [27]
The Introduction reports bacteriophages in the complex cheese starter culture and identifies phage predation as part of the basis for its resilience. The Discussion says phage predation preserves strain diversity by suppressing abundant strains, while the study also documents variation in phage sensitivity. It does not establish that phages generate new genetic and phenotypic diversity, rather than help maintain existing diversity. (LLM, conf=0.85)
Experimental — accuracy not yet measuredFluctuations in plasmid content among natural communities give rise to subpopulations that offer selective advantages in the face of environmental uncertainty.
“Thus, fluctuations in plasmid content among natural communities give rise to subpopulations that offer selective advantages in the face of environmental uncertainty [27].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [27]
The "kill the winner" model explains how strong duplication of a specific strain within a microbial community triggers a corresponding increase in viral populations that target that strain, resulting in a reduction in the population size of the rapidly growing strain, ultimately promoting diversity within the overall community.
“In this context, the “kill the winner” model is intriguing. It explains how the strong duplication of a specific strain within a microbial community triggers a corresponding increase in viral populations that target that strain. This results in a reduction in the population size of the rapidly growing strain, ultimately promoting diversity within the overall community [27].”
From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [27]
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Cites
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
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010) · Systematic Biology · doi:10.1093/sysbio/syq010 · Cited by 18,376 · see citing works
The RAST Server: Rapid Annotations using Subsystems Technology
Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T. L., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., et al. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-75 · Cited by 11,777 · see citing works
A human gut microbial gene catalogue established by metagenomic sequencing
MetaHIT Consortium, Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., et al. (2010) · Nature · doi:10.1038/nature08821 · Cited by 11,624 · see citing works
Genome sequencing in microfabricated high-density picolitre reactors
Margulies, M., Egholm, M., Altman, W. E., Attiya, S., Bader, J. S., Bemben, L. A., Berka, J., Braverman, M. S., Chen, Y.-J., Chen, Z., et al. (2005) · Nature · doi:10.1038/nature03959 · Cited by 7,693 · see citing works
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
Li, L., Stoeckert, C. J., & Roos, D. S. (2003) · Genome Research · doi:10.1101/gr.1224503 · Cited by 5,707 · see citing works
Metagenomic Analysis of the Human Distal Gut Microbiome
Gill, S. R., Pop, M., DeBoy, R. T., Eckburg, P. B., Turnbaugh, P. J., Samuel, B. S., Gordon, J. I., Relman, D. A., Fraser-Liggett, C. M., & Nelson, K. E. (2006) · Science · doi:10.1126/science.1124234 · Cited by 4,699 · see citing works
MEGAN analysis of metagenomic dataPreprint
Huson, D. H., Auch, A. F., Qi, J., & Schuster, S. C. (2007) · Genome Research · doi:10.1101/gr.5969107 · Cited by 3,293 · see citing works
Scaffolding pre-assembled contigs using SSPACE.
Boetzer, M., Henkel, C. V., Jansen, H. J., Butler, D., & Pirovano, W. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btq683 · Cited by 2,337 · see citing works
A Whole-Genome Assembly of Drosophila
Myers, E. W., Sutton, G. G., Delcher, A. L., Dew, I. M., Fasulo, D., Flanigan, M. J., Kravitz, S. A., Mobarry, C. M., Reinert, K., Remington, K., et al. (2000) · Science · doi:10.1126/science.287.5461.2196 · Cited by 1,533 · see citing works
Comparative genomics of the lactic acid bacteria.
Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607117103 · Cited by 1,391 · see citing works
Surviving the Acid Test: Responses of Gram-Positive Bacteria to Low pH
Cotter, P. D., & Hill, C. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.3.429-453.2003 · Cited by 1,378 · see citing works
Genomic Islands in Pathogenic and Environmental Microorganisms
Dobrindt, U., Hochhut, B., Hentschel, U., & Hacker, J. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro884 · Cited by 1,188 · see citing works
The Complete Genome Sequence of the Lactic Acid Bacterium Lactococcus lactis ssp. lactis IL1403
Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., Ehrlich, S. D., & Sorokin, A. (2001) · Genome Research · doi:10.1101/gr.gr-1697r · Cited by 1,139 · see citing works
The Complete Genome Sequence of the Lactic Acid Bacterium Lactococcus lactis ssp. lactis IL1403Preprint
Bolotin, A., Wincker, P., Mauger, S., Jaillon, O., Malarme, K., Weissenbach, J., Ehrlich, S. D., & Sorokin, A. (2001) · Genome Research · doi:10.1101/gr.169701 · Cited by 1,133 · see citing works
Thingstad, T. F. (2000) · Limnology and Oceanography · doi:10.4319/lo.2000.45.6.1320 · Cited by 1,085 · see citing works
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 · see citing works
The proteotytic systems of lactic acid bacteria
Kunji, E. R. S., Mierau, I., Hagting, A., Poolman, B., & Konings, W. N. (1996) · Antonie van Leeuwenhoek · doi:10.1007/bf00395933 · Cited by 715 · see citing works
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 · see citing works
Bennett, S. T. (2004) · Pharmacogenomics · doi:10.1517/14622416.5.4.433 · Cited by 618 · see citing works
Antagonistic activities of lactic acid bacteria in food and feed fermentations
Lindgren, S., & Dobrogosz, W. J. (1990) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.1990.tb04885.x · Cited by 585 · see citing works
Metagenomic Analysis of Kimchi, a Traditional Korean Fermented Food
Jung, J. Y., Lee, S. H., Kim, J. M., Park, M. S., Bae, J., Hahn, Y., Madsen, E. L., & Jeon, C. O. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02157-10 · Cited by 484 · see citing works
Viral and microbial community dynamics in four aquatic environments
Rodriguez-Brito, B., Li, L., Wegley, L., Furlan, M., Angly, F. E., Breitbart, M., Buchanan, J. T., Desnues, C., Dinsdale, E. A., Edwards, R. A., et al. (2010) · The ISME Journal · doi:10.1038/ismej.2010.1 · Cited by 430 · see citing works
Wegmann, U., Motherway, M. O., Zomer, A., Buist, G., Shearman, C. A., Canchaya, C. A., Ventura, M., Goesmann, A., Gasson, M. J., Kuipers, O. P., et al. (2007) · Journal of Bacteriology · doi:10.1128/jb.01768-06 · Cited by 418 · see citing works
Randazzo, C. L., Torriani, S., Akkermans, A. D. L., de Vos, W. M., & Vaughan, E. E. (2002) · Applied and Environmental Microbiology · doi:10.1128/aem.68.4.1882-1892.2002 · Cited by 367 · see citing works
Prokaryotic Genetic Diversity throughout the Salinity Gradient of a Coastal Solar Saltern
Benlloch, S., López‐López, A., Casamayor, E. O., Øvreås, L., Goddard, V., Daae, F. L., Smerdon, G., Massana, R., Joint, I., Thingstad, F., et al. (2002) · Environmental Microbiology · doi:10.1046/j.1462-2920.2002.00306.x · Cited by 316 · see citing works
A chloride‐inducible acid resistance mechanism in Lactococcus lactis and its regulation
Sanders, J.-W., Leenhouts, K. J., Burghoorn, J., Brands, J. R., Venema, G., & Kok, J. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.00676.x · Cited by 276 · see citing works
Buckenhüskes, H. J. (1993) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.1993.tb00022.x · Cited by 274 · see citing works
The identification of functional modules from the genomic association of genes
Snel, ., Peer Bork, B., & Huynen, M. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.092632599 · Cited by 248 · see citing works
Delbès, C., Ali-Mandjee, L., & Montel, M. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01716-06 · Cited by 230 · see citing works
Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria
Penn, K., Jenkins, C., Nett, M., Udwary, D., Gontang, E. A., McGlinchey, R. P., Foster, B., Lapidus, A. L., Podell, S. B., Allen, E. E., et al. (2009) · The ISME Journal · doi:10.1038/ismej.2009.58 · Cited by 203 · see citing works
iPath: interactive exploration of biochemical pathways and networks
Letunić, I., Yamada, T., Kanehisa, M. I., & Peer Bork, B. (2008) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2008.01.001 · Cited by 201 · see citing works
Siezen, R. J., Renckens, B., van Swam, I. I., Peters, S., van Kranenburg, R., Kleerebezem, M., & de Vos, W. M. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8371-8382.2005 · Cited by 145 · see citing works
Self-citationIntraspecific genotypic richness and relatedness predict the invasibility of microbial communities
Jousset, A., Schulz, W., Scheu, S., & Eisenhauer, N. (2011) · The ISME Journal · doi:10.1038/ismej.2011.9 · Cited by 142 · see citing works
Lilley, A. K., & Bailey, M. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.4.1577-1583.1997 · Cited by 140 · see citing works
Systems Solutions by Lactic Acid Bacteria: From Paradigms to Practice
de Vos, W. M. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-s1-s2 · Cited by 134 · see citing works
Siezen, R. J., Starrenburg, M. J. C., Boekhorst, J., Renckens, B., Douwe Molenaar, B., & Vlieg, J. E. T. V. H. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.01850-07 · Cited by 128 · see citing works
Siezen, R. J., Bayjanov, J. R., Renckens, B., Wels, M., van Hijum, S. A. F. T., Douwe Molenaar, B., & Vlieg, J. E. T. V. H. (2010) · Journal of Bacteriology · doi:10.1128/jb.00276-10 · Cited by 112 · see citing works
Plasmids of lactococci – genetic accessories or genetic necessities?
Mills, S., McAuliffe, O. E., Coffey, A., Fitzgerald, G. F., & Ross, R. P. (2006) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2005.00011.x · Cited by 98 · see citing works
Diversity of lactic acid bacteria in two Flemish artisan raw milk Gouda-type cheeses
Hoorde, K. V., Verstraete, T., Vandamme, P. A. R., et al. (2008) · Food Microbiology · doi:10.1016/j.fm.2008.06.006 · Cited by 97 · see citing works
Monnet, C., Loux, V., Gibrat, J.-F., Spinnler, H.-É., Barbe, V., Vacherie, B., Gavory, F., Gourbeyre, E., Siguier, P., Chandler, M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015489 · Cited by 92 · see citing works
Schröder, J., Maus, I., Trost, E., & Tauch, A. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-545 · Cited by 76 · see citing works
Lilley, A. K., & Bailey, M. (1997) · Applied and Environmental Microbiology · doi:10.1128/aem.63.4.1584-1587.1997 · Cited by 67 · see citing works
Heuer, H., Abdo, Z., & Smalla, K. (2008) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2008.00539.x · Cited by 64 · see citing works
High 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 · see citing works
Self-citationCharacterization of Lactococcus lactis Phage 949 and Comparison with Other Lactococcal Phages
Samson, J. E., & Moineau, S. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00796-10 · Cited by 56 · see citing works
Selection 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 · see citing works
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 · see citing works
Self-citationFeirtag, J. M., Petzel, J. P., Pasalodos, E., et al. (1991) · Applied and Environmental Microbiology · doi:10.1128/aem.57.2.539-548.1991 · Cited by 24 · see citing works
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 · see citing works
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Marco, M. L., Heeney, D., Binda, S., Cifelli, C. J., Cotter, P. D., Foligné, B., Gänzle, M., Kort, R., Pasin, G., Pihlanto, A., et al. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2016.11.010 · Cited by 1,674 · see citing works
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De Filippis, F., Genovese, A., Ferranti, P., Gilbert, J. A., & Ercolini, D. (2016) · Scientific Reports · doi:10.1038/srep21871 · Cited by 196 · see citing works
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Mayo, B., Rachid, C., Alegria, A., Leite, A., Peixoto, R., & Delgado, S. (2014) · Current Genomics · doi:10.2174/1389202915666140616233211 · Cited by 188 · see citing works
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De Filippis, F., Parente, E., & Ercolini, D. (2018) · Annual Review of Food Science and Technology · doi:10.1146/annurev-food-030117-012312 · Cited by 163 · see citing works
Smid, E. J., Erkus, O., Spus, M., Wolkers-Rooijackers, J. C., Alexeeva, S., & Kleerebezem, M. (2014) · Microbial Cell Factories · doi:10.1186/1475-2859-13-s1-s2 · Cited by 117 · see citing works
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Teusink, B., & Molenaar, D. (2017) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2017.07.005 · Cited by 95 · see citing works
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Cocolin, L., & Ercolini, D. (2015) · Current Opinion in Food Science · doi:10.1016/j.cofs.2015.01.003 · Cited by 93 · see citing works
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Schaerer, L. G., Wu, R., Putman, L. I., Pearce, J. M., Lu, T., Shonnard, D. R., Ong, R. G., & Techtmann, S. M. (2023) · Trends in Biotechnology · doi:10.1016/j.tibtech.2022.06.012 · Cited by 52 · see citing works
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“Thus, fluctuations in plasmid content among natural communities give rise to subpopulations that offer selective advantages in the face of environmental uncertainty [27].”
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- Authors
- 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.
- Affiliations
- Laboratory of Microbiology, Wageningen University , Wageningen, Netherlands
- TiFN (NL)
- NIZO food research BV , Ede, The Netherlands
- Corresponding author
- Smid, Eddy J
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-07-04
- Volume
- 7
- Issue
- 11
- Pages
- 2126-2136
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC3806261
- OpenAlex
- W2074191684
- Cited by
- 217
- References
- 52
- Citations by year
- 2026: 5 · 2025: 15 · 2024: 23 · 2023: 24 · 2022: 19 · 2021: 17 · 2020: 22 · 2019: 13 · 2018: 13 · 2017: 20 · 2016: 20 · 2015: 15 · 2014: 9 · 2013: 1
- FWCI
- 9.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The ISME Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- microbial community stability, cheese starter cultures, Lactococcus lactis, Leuconostoc mesenteroides, genetic lineages, plasmid content, phage predation, density-dependent selection, backslopping, genetic heterogeneity, biodiversity maintenance, environmental uncertainty
- MeSH terms
- Bacteriophages, Cheese, Food Microbiology, Leuconostoc, Plasmids, RNA, Ribosomal, 16S, Lactococcus lactis, Genetic Variation, Genome, Bacterial
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