Cited by 55Bacteriophages and microbial interactionsProbiotics and Fermented FoodsEvolution and Genetic Dynamics

Functional Strain Redundancy and Persistent Phage Infection in Swiss Hard Cheese Starter Cultures

Open access
Somerville, Vincent, Berthoud, Hélène, Schmidt, Remo S, Bachmann, Hans-Peter, Meng, Yi Hélène, Fuchsmann, Pascal, von Ah, Ueli, Engel, Philipp·2022·The ISME Journal

Published version of a preprint

Abstract

Undefined starter cultures are poorly characterized bacterial communities from environmental origin used in cheese making. They are phenotypically stable and have evolved through domestication by repeated propagation in closed and highly controlled environments over centuries. This makes them interesting for understanding eco-evolutionary dynamics governing microbial communities. While cheese starter cultures are known to be dominated by a few bacterial species, little is known about the composition, functional relevance, and temporal dynamics of strain-level diversity. Here, we applied shotgun metagenomics to an important Swiss cheese starter culture and analyzed historical and experimental samples reflecting 82 years of starter culture propagation. We found that the bacterial community is highly stable and dominated by only a few coexisting strains of Streptococcus thermophilus and Lactobacillus delbrueckii subsp. lactis. Genome sequencing, metabolomics analysis, and co-culturing experiments of 43 isolates show that these strains are functionally redundant, but differ tremendously in their phage resistance potential. Moreover, we identified two highly abundant Streptococcus phages that seem to stably coexist in the community without any negative impact on bacterial growth or strain persistence, and despite the presence of a large and diverse repertoire of matching CRISPR spacers. Our findings show that functionally equivalent strains can coexist in domesticated microbial communities and highlight an important role of bacteria-phage interactions that are different from kill-the-winner dynamics.

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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 [28]

    The Discussion (page not available) says phage interactions may help maintain strain-level diversity and reports new CRISPR spacers acquired during propagation. It does not establish that phages drive phenotypic diversity or that their presence causes the resistance described in the claim; the paper describes the coexisting strains as functionally redundant. (LLM, conf=0.87)

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  • High functional redundancy of strains in Swiss hard cheese starter cultures ensures product stability, while strain-level variability provides adaptability to environmental changes.

    “The high functional redundancy of strains in these cultures ensures product stability, while strain-level variability provides adaptability to environmental changes of various natures.”

    From Microbiota of Cheese Ecosystems: A Perspective on Cheesemaking (2025) · cites this paper as [28]

    The Results section on phenotypic redundancy reports that strains were functionally redundant in important cheese-making properties, and the Discussion describes similar traits across isolates. But the Introduction says the reason for greater starter-culture stability is unknown and presents resilience to environmental stressors only as a possibility. The paper therefore does not establish that redundancy ensures product stability or that strain-level variability provides adaptability to environmental changes generally. (LLM, conf=0.87)

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Research works printed but not linked: 1

  1. [4]Powell IB Broome MC Limsowtin GKY Reference Module in Food Science 2016 London Elsevier

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Authors
Somerville, V., Berthoud, H., Schmidt, R. S., Bachmann, H.-P., Meng, Y. H., Fuchsmann, P., von Ah, U., & Engel, P.
Affiliations
  • Agroscope (CH)
  • Agroscope , Bern, Switzerland
  • University of Lausanne (CH)
Corresponding author
  • Somerville, Vincent
  • Engel, Philipp
Venue
The ISME Journal
Published
2021-08-06
Volume
16
Issue
2
Pages
388-399
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
OpenAlex
W3190617484
Cited by
55
References
110
Citations by year
2026: 8 · 2025: 13 · 2024: 14 · 2023: 8 · 2022: 11 · 2021: 1
FWCI
4.59
Type
journal article
Language
en
Open access
Locations
  • The ISME Journal (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • SERVAL (Université de Lausanne) (publishedVersion, cc-by)
  • IRIS (submittedVersion, cc-by)
Funders
  • Université de Lausanne
  • Agroscope, Liebefeld, Switzerland
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (51NF40_180575, 31003A_179487)
Topics
  • Physical Sciences › Environmental Science › Ecology › Bacteriophages and microbial interactions
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
cheese starter cultures, phage infection, Streptococcus thermophilus, Lactobacillus delbrueckii subsp. lactis, phage resistance, CRISPR spacers, eco-evolutionary dynamics, microbial community stability, strain-level diversity
MeSH terms
Bacteria, Bacteriophages, Food Microbiology, Metagenomics, Microbiota

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