Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Somerville, Vincent; Berthoud, Hélène; Schmidt, Roman; Bachmann, H; Meng, Yi; Fuchsmann, Pascal; Ah, Ueli von; Engel, Philipp

doi:10.1101/2021.01.14.426499

Cited by 4 publications

(5 citation statements)

References 99 publications

(88 reference statements)

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“…18). This observation is in contrast to what has been observed in laboratory studies of phage-bacteria coevolution (36,45) or in cases of chronic phage infections in S. thermophilus (31), where multiple spacers targeting the same vOTU were often found to be integrated into the CRISPR array.…”

Section: No Complete Pan-immunity By Crispr Defensecontrasting

confidence: 96%

“…Indeed, previous estimates of CRISPR acquisition rates based on experimental data were ~1 magnitude lower (<0.1 spacer/generation in (31) or ~0.5 spacer/generation in ( 34)).…”

Section: Rapid Turnover Of Crispr Spacers In Nearly Identical Strains...mentioning

confidence: 92%

“…Notably, in our previous study focusing on a single cheese starter culture we had found the opposite pattern. This may be explained by the fact that a single phage dominated this community, causing chronic infections and thereby overcoming CRISPR-based immunity (31).…”

Section: Crispr Spacer Abundances Correlates With Target Abundancementioning

confidence: 99%

“…In order to analyze species and CRISPR diversity in cheese related samples we gathered 158 shotgun metagenomic samples and 322 16S metagenomic samples from overall 18 studies from NCBI (see Suppl. table 1) (31,(54)(55)(56)(57)(58)(59)(60)(61)(62)(63)(64)(65)(66)(67)(68).…”

Section: Metagenomesmentioning

confidence: 99%

“…This makes them tractable systems to study the evolution of phage defense systems in microbial communities at the strain-level (29,30). Indeed, our previous study of a single Swiss cheese starter culture has shown that extensive intraspecific CRISPR spacer diversity exists in these otherwise nearly clonal populations of bacteria (31).…”

mentioning

confidence: 99%

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Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

Somerville

Schowing

Chabas

et al. 2022

Preprint

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Phages are key drivers of genomic diversity in bacterial populations as they impose strong selective pressure on the evolution of bacterial defense mechanisms across closely related strains. The pan-immunity model suggests that such diversity is maintained because the effective immune system of a bacterial species is the one distributed across all strains present in the community. However, only few studies have analyzed the distribution of bacterial defense systems at the community-level, mostly focusing on CRISPR and comparing samples from complex environments. Here, we studied 2'778 bacterial genomes and 158 metagenomes from cheese-associated communities, which are dominated by a few bacterial taxa and occur in relatively stable environments. We find that nearly identical strains of cheese-associated bacteria contain diverse and highly variable arsenals of innate and adaptive (i.e CRISPR-Cas) immunity suggesting rapid turnover of defense mechanisms in these communities. CRISPR spacer abundance correlated with the abundance of matching target sequences across the metagenomes providing evidence that the identified defense repertoires are functional and under selection. While these characteristics align with the pan-immunity model, the detected CRISPR spacers only covered a subset of the phages previously identified in cheese, suggesting that CRISPR does not provide complete immunity against all phages, and that the innate immune mechanisms may have complementary roles. Our findings show that the evolution of bacterial defense mechanisms is a highly dynamic process and highlight that experimentally tractable, low complexity communities such as those found in cheese, can help to understand ecological and molecular processes underlying phage-defense system relationships.

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Section: No Complete Pan-immunity By Crispr Defensecontrasting

confidence: 96%

“…Indeed, previous estimates of CRISPR acquisition rates based on experimental data were ~1 magnitude lower (<0.1 spacer/generation in (31) or ~0.5 spacer/generation in ( 34)).…”

Section: Rapid Turnover Of Crispr Spacers In Nearly Identical Strains...mentioning

confidence: 92%

Section: Crispr Spacer Abundances Correlates With Target Abundancementioning

confidence: 99%

Section: Metagenomesmentioning

confidence: 99%

mentioning

confidence: 99%

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Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

Somerville

Schowing

Chabas

et al. 2022

Preprint

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Dynamics of the viral community on the surface of a French smear-ripened cheese during maturation and persistence across production years

Paillet,

Lamy-Besnier,

Figueroa

et al. 2023

Preprint

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The surface of smear-ripened cheeses constitutes a dynamic microbial ecosystem resulting from the successive development of different microbial groups. Recent studies indicate that a viral community, mainly composed of bacteriophages, coexists with cellular microorganisms in this ecosystem, but its ecological significance remains to be elucidated. In this work, we studied a French smear-ripened cheese by both viral metagenomics and 16S metabarcoding approaches to assess both the dynamics of phages and bacterial communities on the cheese surface during the ripening period, and their persistence in ready-to-eat cheeses over the years of production. We observed a clear transition of the phage community structure during ripening with a decreased relative abundance of viral species (vOTUs) associated withLactococcusphages, which were replaced by vOTUs associated with phages infecting ripening bacteria such asBrevibacterium, Glutamicibacter, PseudoalteromonasandVibrio. The dynamics of the phage community was strongly associated with bacterial successions observed on the cheese surface. Finally, a core of abundant vOTUs were systematically detected in ready-to-eat cheeses produced at different dates spanning more than 4 years of production, indicating long-term persistence of the main phages in the cheese production environment. Together, these findings offer novel perspectives on the ecology of bacteriophages in smear-ripened cheese and emphasize the significance of incorporating bacteriophages in the microbial ecology studies of fermented foods.IMPORTANCESmear-ripened cheeses are microbial ecosystems made up of various microorganisms including bacteria, yeasts and also viruses such as bacteriophages, which infect and regulate bacterial populations. In this work, a French smear-ripened cheese was used to study how these viruses and bacteria interact over time and during cheese production. It revealed that the composition of the bacteriophage community shifts during the ripening process, aligning with the bacterial successions observed on the cheese surface between lactic acid bacteria and ripening bacteria. Additionally, the vast majority of these bacteriophages were found consistently in cheese products made over a 4-years period, showing that they represent a persistent component of the cheese-making environment. This research highlights the importance of considering these bacteriophages when studying the microbial life of fermented foods like cheese.

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Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

et al. 2022

Self Cite

View full text Add to dashboard Cite

Background Phages are key drivers of genomic diversity in bacterial populations as they impose strong selective pressure on the evolution of bacterial defense mechanisms across closely related strains. The pan-immunity model suggests that such diversity is maintained because the effective immune system of a bacterial species is the one distributed across all strains present in the community. However, only few studies have analyzed the distribution of bacterial defense systems at the community-level, mostly focusing on CRISPR and comparing samples from complex environments. Here, we studied 2778 bacterial genomes and 188 metagenomes from cheese-associated communities, which are dominated by a few bacterial taxa and occur in relatively stable environments. Results We corroborate previous laboratory findings that in cheese-associated communities nearly identical strains contain diverse and highly variable arsenals of innate and adaptive (i.e., CRISPR-Cas) immunity systems suggesting rapid turnover. CRISPR spacer abundance correlated with the abundance of matching target sequences across the metagenomes providing evidence that the identified defense repertoires are functional and under selection. While these characteristics align with the pan-immunity model, the detected CRISPR spacers only covered a subset of the phages previously identified in cheese, providing evidence that CRISPR does not enable complete immunity against all phages, and that the innate immune mechanisms may have complementary roles. Conclusions Our findings show that the evolution of bacterial defense mechanisms is a highly dynamic process and highlight that experimentally tractable, low complexity communities such as those found in cheese, can help to understand ecological and molecular processes underlying phage-defense system relationships. These findings can have implications for the design of robust synthetic communities used in biotechnology and the food industry.

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Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures

Cited by 4 publications

References 99 publications

Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

Dynamics of the viral community on the surface of a French smear-ripened cheese during maturation and persistence across production years

Extensive diversity and rapid turnover of phage defense repertoires in cheese-associated bacterial communities

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