Cell Wall Glycans Mediate Recognition of the Dairy Bacterium Streptococcus thermophilus by Bacteriophages

Szymczak, Paula; Filipe, Sérgio R.; Covas, Gonçalo; Vogensen, Finn K.; Neves, Ana Rute; Janzen, Thomas

doi:10.1128/aem.01847-18

Cited by 32 publications

(31 citation statements)

References 69 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Another study demonstrated that transient inactivation of the CRISPR-Cas system allows isolation of non-CRISPR-mediated bacteriophage insensitive mutants (BIMs) 27 . Characterization of these non-CRISPR BIMs offers the possibility of identifying new bacterial factors that can be mutated to reduce phage infection such as the newly described mutations in cell wall glycans 28 .…”

Section: Introductionmentioning

confidence: 99%

A mutation in the methionine aminopeptidase gene provides phage resistance in Streptococcus thermophilus

Labrie

Mosterd

Loignon

et al. 2019

Sci Rep

View full text Add to dashboard Cite

Streptococcus thermophilus is a lactic acid bacterium widely used by the dairy industry for the manufacture of yogurt and specialty cheeses. It is also a Gram-positive bacterial model to study phage-host interactions. CRISPR-Cas systems are one of the most prevalent phage resistance mechanisms in S. thermophilus. Little information is available about other host factors involved in phage replication in this food-grade streptococcal species. We used the model strain S. thermophilus SMQ-301 and its virulent phage DT1, harboring the anti-CRISPR protein AcrIIA6, to show that a host gene coding for a methionine aminopeptidase (metAP) is necessary for phage DT1 to complete its lytic cycle. A single mutation in metAP provides S. thermophilus SMQ-301 with strong resistance against phage DT1. The mutation impedes a late step of the lytic cycle since phage adsorption, DNA replication, and protein expression were not affected. When the mutated strain was complemented with the wild-type version of the gene, the phage sensitivity phenotype was restored. When this mutation was introduced into other S. thermophilus strains it provided resistance against cos-type (Sfi21dt1virus genus) phages but replication of pac-type (Sfi11virus genus) phages was not affected. The mutation in the gene coding for the MetAP induces amino acid change in a catalytic domain conserved across many bacterial species. Introducing the same mutation in Streptococcus mutans also provided a phage resistance phenotype, suggesting the wide-ranging importance of the host methionine aminopeptidase in phage replication.

show abstract

Section: Introductionmentioning

confidence: 99%

A mutation in the methionine aminopeptidase gene provides phage resistance in Streptococcus thermophilus

Labrie

Mosterd

Loignon

et al. 2019

Sci Rep

View full text Add to dashboard Cite

show abstract

“…6%), however, encoded functions related to amino acid transport and polysaccharide biosynthesis ( Supplementary Fig. 11), including eight glycosyl-and sugar transferase genes involved in cell wall modifications of S. thermophilus and known for their role in phage resistance 25,26 . The genomes from different lineages were largely syntenic ( Supplementary Fig.…”

Section: Thermophilus Strainsmentioning

confidence: 99%

“…The exceedingly high numbers of phage copies suggest an ongoing proliferation of the phage most likely from a temperate source. Given the high abundance of the two phages in the starter cultures, despite the prevalence of matching CRISPR spacers, we assume that the phages can evade the CRISPR defense system 26,38 . In both phage genomes we found genes encoding the anti-CRISPR (Acr) proteins AcrIIA3 39 and AcrIIA6 40 known to inhibit CRISPR-CAS complexes and their defensive function (Fig.…”

Section: Highly Variable Phage Resistance Mechanisms In Isolated Genomesmentioning

confidence: 99%

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

Somerville

Berthoud

Schmidt

et al. 2021

Preprint

View full text Add to dashboard Cite

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.

show abstract

“…The selection of these mutants suggests taking advantage of different phage resistance mechanisms. For example, some of them may have mutations at the phage receptor level (19) or other host factors (20). However, many of these BIMs are obtained via their CRISPR-Cas systems (21).…”

mentioning

confidence: 99%

Novel Genus of Phages Infecting Streptococcus thermophilus: Genomic and Morphological Characterization

Philippe

Levesque

Dion

et al. 2020

Appl Environ Microbiol

View full text Add to dashboard Cite

Streptococcus thermophilus is a lactic acid bacterium commonly used for the manufacture of yogurt and specialty cheeses. Virulent phages represent a major risk for milk fermentation processes worldwide, as they can inactivate the added starter bacterial cells, leading to low-quality fermented dairy products. To date, four genetically distinct groups of phages infecting S. thermophilus have been described. Here, we describe a fifth group. Phages P738 and D4446 are virulent siphophages that infect a few industrial strains of S. thermophilus. The genomes of phages P738 and D4446 were sequenced and found to contain 34,037 and 33,656 bp as well as 48 and 46 open reading frames, respectively. Comparative genomic analyses revealed that the two phages are closely related to each other but display very limited similarities to other S. thermophilus phages. In fact, these two novel S. thermophilus phages share similarities with streptococcal phages of nondairy origin, suggesting that they emerged recently in the dairy environment. IMPORTANCE Despite decades of research and adapted antiphage strategies such as CRISPR-Cas systems, virulent phages are still a persistent risk for the milk fermentation industry worldwide, as they can cause manufacturing failures and alter product quality. Phages P738 and D4446 are novel virulent phages that infect the food-grade Gram-positive bacterial species Streptococcus thermophilus. These two related viruses represent a fifth group of S. thermophilus phages, as they are significantly distinct from other known S. thermophilus phages. Both phages share similarities with phages infecting nondairy streptococci, suggesting their recent emergence and probable coexistence in dairy environments. These findings highlight the necessity of phage surveillance programs as the phage population evolves in response to the application of antiphage strategies.

show abstract

Cell Wall Glycans Mediate Recognition of the Dairy Bacterium Streptococcus thermophilus by Bacteriophages

Cited by 32 publications

References 69 publications

A mutation in the methionine aminopeptidase gene provides phage resistance in Streptococcus thermophilus

A mutation in the methionine aminopeptidase gene provides phage resistance in Streptococcus thermophilus

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

Novel Genus of Phages Infecting Streptococcus thermophilus: Genomic and Morphological Characterization

Contact Info

Product

Resources

About