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.
Change History: September 2019 The title of the chapter has been adapted from Propionibacterium spp. to Propionibacterium spp. and Acidipropionibacterium spp., due to adaptions in the classification. The authorship has been expanded. Overall, the term "Emmental" has been replaced by the generic term "Swiss-type cheese". MT Fröhlich-Wyder and A Thierry revised the 'Introduction' section. U von Ah updated the 'Classification and Identification' section, described the new genus Acidipropionibacterium and Propionibacteriaceae family, added Table 1 as a new Table and updated Table 2 (from the Table 1 of the previous version). A Thierry and SM Deutsch revised and enriched the 'Morphology, Envelopes and Growth Conditions' section. M Turgay largely extended and updated the section 'Genetics', renamed into 'Genetic properties', from new complete genome sequence data, added Table 3 as a new Table, and updated Table 4 (from Table 2 of the previous version), replaced Table 3 by an extended section 'Genetic engineering' and added a section 'Immunity'. S Irmler restructured and enriched the section 'Metabolism' with short information on the biosynthesis of vitamin B12, trehalose, and pigment and additional information on the conversion of aspartate into succinate and modified Figure 1. G Jan updated and edited the section 'Adaptation to Stress'. MT Fröhlich-Wyder updated the section 'Use as Ripening Cultures in Cheese'. G Jan and H Falentin updated and edited the section 'Relation to Nutrition as Probiotics and Producers of Nutraceuticals'. HP Bachmann expanded the section 'Antimicrobial activities' into a section entitled 'Use as Protective Cultures' and updated Table 5 (from the Table 4 of the previous version). This is an update of A.
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