Complete Genome Sequences of Bacteriocin-Producing Streptococcus thermophilus Strains ST106 and ST109

Renye, John A.; Needleman, David S.; Steinberg, Dennis H.

doi:10.1128/mra.01336-18

Cited by 6 publications

(10 citation statements)

References 13 publications

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“…Finally, the pan genome of the species is not closed yet, suggesting that sequencing of additional strains will be important. Certain new complete genomes have appeared in the databases since the initiation of our analysis (Proust et al, 2018;Renye et al, 2019), but more are required to further expand and validate any lineage-like patterns that may exist and could be related to the technological/probiotic repertoire of S. thermophilus.…”

Section: Resultsmentioning

confidence: 99%

Comparative Genomics of Streptococcus thermophilus Support Important Traits Concerning the Evolution, Biology and Technological Properties of the Species

et al. 2019

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Streptococcus thermophilus is a major starter for the dairy industry with great economic importance. In this study we analyzed 23 fully sequenced genomes of S. thermophilus to highlight novel aspects of the evolution, biology and technological properties of this species. Pan/core genome analysis revealed that the species has an important number of conserved genes and that the pan genome is probably going to be closed soon. According to whole genome phylogeny and average nucleotide identity (ANI) analysis, most S. thermophilus strains were grouped in two major clusters (i.e., clusters A and B). More specifically, cluster A includes strains with chromosomes above 1.83 Mbp, while cluster B includes chromosomes below this threshold. This observation suggests that strains belonging to the two clusters may be differentiated by gene gain or gene loss events. Furthermore, certain strains of cluster A could be further subdivided in subgroups, i.e., subgroup I (ASCC 1275, DGCC 7710, KLDS SM, MN-BM-A02, and ND07), II (MN-BM-A01 and MN-ZLW-002), III (LMD-9 and SMQ-301), and IV (APC151 and ND03). In cluster B certain strains formed one distinct subgroup, i.e., subgroup I (CNRZ1066, CS8, EPS, and S9). Clusters and subgroups observed for S. thermophilus indicate the existence of lineages within the species, an observation which was further supported to a variable degree by the distribution and/or the architecture of several genomic traits. These would include exopolysaccharide (EPS) gene clusters, Clustered Regularly Interspaced Short Palindromic Repeats (CRISPRs)-CRISPR associated (Cas) systems, as well as restriction-modification (R-M) systems and genomic islands (GIs). Of note, the histidine biosynthetic cluster was found present in all cluster A strains (plus strain NCTC12958 T) but was absent from all strains in cluster B. Other loci related to lactose/galactose catabolism and urea metabolism, aminopeptidases, the majority of amino acid and peptide transporters, as well as amino acid biosynthetic pathways

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Section: Resultsmentioning

confidence: 99%

Comparative Genomics of Streptococcus thermophilus Support Important Traits Concerning the Evolution, Biology and Technological Properties of the Species

et al. 2019

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“…The genomes of strains ST106 ( Renye et al, 2019a ) and B59671 ( Renye et al, 2017 ) were completely sequenced in previous studies. Analysis of the RNA-seq data was performed using Geneious Prime software (Biomatters Inc., Boston, MA, United States) and by Igenbio Inc. using their proprietary ERGO 2.0 platform.…”

Section: Methodsmentioning

confidence: 99%

“…Many of the bacteriocins produced from S. thermophilus , called thermophilins, are encoded by the bacteriocin-like peptide ( blp ) gene cluster. Strains B59671 ( Gilbreth and Somkuti, 2005 ; Renye and Somkuti, 2013 ), ST106 ( Somkuti and Renye, 2014 ; Renye et al, 2019a ; Figure 1A ), LMD-9 ( Fontaine et al, 2007 ; Fontaine and Hols, 2008 ), ST109 ( Renye et al, 2019b ), and ST118 ( Somkuti and Renye, 2014 ) all produce bacteriocins encoded within the blp cluster. The blp -encoded bacteriocins produced by ST106 and B59671 are called thermophilin 106 and thermophilin 110, respectively.…”

Section: Introductionmentioning

confidence: 99%

The quorum sensing peptide BlpC regulates the transcription of genes outside its associated gene cluster and impacts the growth of Streptococcus thermophilus

McAnulty,

Guron,

Oest

et al. 2024

Front. Microbiol.

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Bacteriocin production in Streptococcus thermophilus is regulated by cell density-dependent signaling molecules, including BlpC, which regulates transcription from within the bacteriocin-like peptide (blp) gene cluster. In some strains, such as S. thermophilus ST106, this signaling system does not function properly, and BlpC must be supplied exogenously to induce bacteriocin production. In other strains, such as S. thermophilus B59671, bacteriocin (thermophilin 110 in strain B59671) production occurs naturally. Here, transcriptomic analyses were used to compare global gene expression within ST106 in the presence or absence of synthetic BlpC and within B59671 to determine if BlpC regulates the expression of genes outside the blp cluster. Real-time semi-quantitative PCR was used to find genes differentially expressed in the absence of chromosomal blpC in the B59671 background. Growth curve experiments and bacteriocin activity assays were performed with knockout mutants and BlpC supplementation to identify effects on growth and bacteriocin production. In addition to the genes involved in bacteriocin production, BlpC affected the expression of several transcription regulators outside the blp gene cluster, including a putative YtrA-subfamily transcriptional repressor. In strain B59671, BlpC not only regulated the expression of thermophilin 110 but also suppressed the production of another bacteriocin, thermophilin 13, and induced the same YtrA-subfamily transcriptional repressor identified in ST106. Additionally, it was shown that the broad-spectrum antimicrobial activity associated with strain B59671 was due to the production of thermophilin 110, while thermophilin 13 appears to be a redundant system for suppressing intraspecies growth. BlpC production or induction negatively affected the growth of strains B59671 and ST106, revealing selective pressure to not produce bacteriocins that may explain bacteriocin production phenotype differences between S. thermophilus strains. This study identifies additional genes regulated by BlpC and assists in defining conditions to optimize the production of bacteriocins for applications in agriculture or human and animal health.

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“…Further analysis of LMD-9 revealed that BlpD alone was sufficient to inhibit the growth of most target bacteria, with BlpU, E, and F identified as accessory peptides that broaden the activity spectrum of BlpD ( Fontaine and Hols, 2008 ). The presence of BlpD in strains ST106 and ST109 suggests it is also the primary bacteriocin within these strains ( Somkuti et al, 2015 ; Renye et al, 2019 ). Additional variations within this gene cluster have been reported ( Rossi et al, 2013 ), and more may arise as the number of fully sequenced strains of S. thermophilus increases.…”

Section: Introductionmentioning

confidence: 99%

BlpU is a broad-spectrum bacteriocin in Streptococcus thermophilus

Renye,

Somkuti,

et al. 2024

Front. Microbiol.

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Streptococcus thermophilus strain B59671 naturally produces thermophilin 110, a broad-spectrum bacteriocin encoded within the bacteriocin-like peptide (blp) gene cluster, and thermophilin 13 from a separate chromosomal locus. Analysis of the blp gene cluster revealed two genes, blpU and blpK, as potentially encoding bacteriocins. Deletion of blpK from the B59671 chromosome did not result in a loss of antimicrobial activity against either S. thermophilus ST113 or Pediococcus acidilactici F. A deletion mutant of blpU could not be generated in B59671, but the mature BlpU peptide obtained through overexpression in E. coli BL21 or chemical synthesis inhibited the growth of S. thermophilus strains, Streptococcus mutans UA159, P. acidilactici F, and Listeria innocua GV9 L-S, evidencing as a broad-spectrum bacteriocin that does not require modification for activity. This study also showed that the transcription of blpU was approximately 16-fold higher in B59671 than in an induced culture of S. thermophilus LMD-9, which produces a blp-encoded bacteriocin. The increased expression of BlpU in B59671 may explain the unique antimicrobial spectrum associated with this strain. Additionally, it was shown that a blpC deletion mutant of B59671, which prevents expression of BlpU and BlpK, inhibited the growth of other S. thermophilus strains and Bacillus cereus, suggesting that thermophilin 13 produced by B59671 possessed both intra- and interspecies antimicrobial activity. While this study confirmed that BlpU can function as an independent antimicrobial peptide, further studies are required to determine if BlpK can function independently as a broad-spectrum antimicrobial.

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Complete Genome Sequences of Bacteriocin-Producing Streptococcus thermophilus Strains ST106 and ST109

Cited by 6 publications

References 13 publications

Comparative Genomics of Streptococcus thermophilus Support Important Traits Concerning the Evolution, Biology and Technological Properties of the Species

Comparative Genomics of Streptococcus thermophilus Support Important Traits Concerning the Evolution, Biology and Technological Properties of the Species

The quorum sensing peptide BlpC regulates the transcription of genes outside its associated gene cluster and impacts the growth of Streptococcus thermophilus

BlpU is a broad-spectrum bacteriocin in Streptococcus thermophilus

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