Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus

Bolotin, Alexander; Quinquis, Benoît; Renault, Pierre; Sorokin, Alexeï; Ehrlich, S. Dusko; Kulakauskas, Saulius; Lapidus, Alla; Goltsman, Eugene; Mazur, Michael; Pusch, Gordon D.; Fonstein, Michael; Overbeek, Ross; Kyprides, Nikos; Purnelle, Bénédicte; Prozzi, Deborah; Ngui, Katrina; Masuy, David; Hancy, Frédéric; Burteau, Sophie; Boutry, Marc; Delcour, Jean; Goffeau, André; Hols, Pascal

doi:10.1038/nbt1034

Cited by 454 publications

(502 citation statements)

References 31 publications

(48 reference statements)

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“…Perhaps some of these could contribute to direct contacts between L. bulgaricus and S. thermophilus as visualized by Bolotin et al (9). From a fermentation viewpoint, the exopolysaccharide (eps) gene clusters present in L. bulgaricus (Table 13, which is published as supporting information on the PNAS web site) and S. thermophilus appear highly diverse.…”

Section: Regulatory Functions: Two Siga Homologues and Relatively Fewmentioning

confidence: 95%

The complete genome sequence ofLactobacillus bulgaricusreveals extensive and ongoing reductive evolution

Guchte

Penaud

Grimaldi

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

370

300

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Lactobacillus delbrueckii ssp. bulgaricus (L. bulgaricus) is a representative of the group of lactic acid-producing bacteria, mainly known for its worldwide application in yogurt production. The genome sequence of this bacterium has been determined and shows the signs of ongoing specialization, with a substantial number of pseudogenes and incomplete metabolic pathways and relatively few regulatory functions. Several unique features of the L. bulgaricus genome support the hypothesis that the genome is in a phase of rapid evolution. (i) Exceptionally high numbers of rRNA and tRNA genes with regard to genome size may indicate that the L. bulgaricus genome has known a recent phase of important size reduction, in agreement with the observed high frequency of gene inactivation and elimination; (ii) a much higher GC content at codon position 3 than expected on the basis of the overall GC content suggests that the composition of the genome is evolving toward a higher GC content; and (iii) the presence of a 47.5-kbp inverted repeat in the replication termination region, an extremely rare feature in bacterial genomes, may be interpreted as a transient stage in genome evolution. The results indicate the adaptation of L. bulgaricus from a plant-associated habitat to the stable protein and lactose-rich milk environment through the loss of superfluous functions and protocooperation with Streptococcus thermophilus.bulgaricus) is one of the economically most important representatives of the heterogeneous group of lactic acid bacteria, with a worldwide application in yogurt production. Yogurt has long been recognized as a nutritious, natural, and safe component of a healthy diet and is at the basis of the concept of probiotics (1, 2). A well documented health benefit of the consumption of yogurt containing live L. bulgaricus and Streptococcus thermophilus is an attenuation of lactose intolerance (3). In addition, immune modulation and diarrhea-alleviating effects have been reported (4), and both L. bulgaricus and S. thermophilus have been implicated in these effects (3,5). During yogurt fermentations protocooperation between these two bacteria results in an accelerated acidification, but the mechanisms involved are not completely understood (6).Among the lactic acid bacteria, L. bulgaricus belongs to the acidophilus complex, a group of lactobacilli related to Lactobacillus acidophilus, Lactobacillus johnsonii, and Lactobacillus gasseri, which have been used as probiotic cultures. Although within this group L. bulgaricus is considered unique because of its atypical GC content, until recently the lack of tools for genetic manipulation has severely hampered a more detailed analysis of this organism (7, 8, † †).Here we present the genome sequence of L. bulgaricus strain ATCC11842, originally isolated from bulgarian yogurt by S. OrlaJensen in 1919 (unpublished work). The analysis of this genome and comparison to other members of the acidophilus complex and S. thermophilus (9) have contributed to a more complete understanding of its p...

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Section: Regulatory Functions: Two Siga Homologues and Relatively Fewmentioning

confidence: 95%

The complete genome sequence ofLactobacillus bulgaricusreveals extensive and ongoing reductive evolution

Guchte

Penaud

Grimaldi

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

370

300

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“…adaptation to milk through the loss of carbohydrate catabolism and virulence genes found in pathogenic streptococci (18). S. thermophilus also underwent significant acquisition of nicherelated genes, such as those encoding including cold-shock proteins, copper resistance proteins, proteinases, bacteriocins, and lactose catabolism proteins (18).…”

Section: Significancementioning

confidence: 99%

“…S. thermophilus is a nonpathogenic, thermophilic Gram-positive bacterium used as a starter culture that catabolizes lactose to lactic acid in the syntrophic production of yogurt and various cheeses (18). S. thermophilus encodes up to four CRISPR-Cas systems, two of which (CRISPR1 and CRISPR3) are classified as type II-A systems that are innately active in both acquisition and interference (4,19).…”

mentioning

confidence: 99%

CRISPR-based screening of genomic island excision events in bacteria

Selle

Klaenhammer

Barrangou

2015

Proc. Natl. Acad. Sci. U.S.A.

116

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Genomic analysis of Streptococcus thermophilus revealed that mobile genetic elements (MGEs) likely contributed to gene acquisition and loss during evolutionary adaptation to milk. Clustered regularly interspaced short palindromic repeats-CRISPR-associated genes (CRISPR-Cas), the adaptive immune system in bacteria, limits genetic diversity by targeting MGEs including bacteriophages, transposons, and plasmids. CRISPR-Cas systems are widespread in streptococci, suggesting that the interplay between CRISPRCas systems and MGEs is one of the driving forces governing genome homeostasis in this genus. To investigate the genetic outcomes resulting from CRISPR-Cas targeting of integrated MGEs, in silico prediction revealed four genomic islands without essential genes in lengths from 8 to 102 kbp, totaling 7% of the genome. In this study, the endogenous CRISPR3 type II system was programmed to target the four islands independently through plasmid-based expression of engineered CRISPR arrays. Targeting lacZ within the largest 102-kbp genomic island was lethal to wild-type cells and resulted in a reduction of up to 2.5-log in the surviving population. Genotyping of Lac − survivors revealed variable deletion events between the flanking insertion-sequence elements, all resulting in elimination of the Lac-encoding island. Chimeric insertion sequence footprints were observed at the deletion junctions after targeting all of the four genomic islands, suggesting a common mechanism of deletion via recombination between flanking insertion sequences. These results established that self-targeting CRISPR-Cas systems may direct significant evolution of bacterial genomes on a population level, influencing genome homeostasis and remodeling.CRISPR | lactic acid bacteria | transposons | IS-elements | Cas9

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“…These studies have demonstrated that CO 2 and sodium bicarbonate stimulate growth and exert a marked influence on the metabolic activities of S. thermophilus. In analyses of the bacterial genome of two strains (Bolotin et al, 2004;Hols et al, 2005), there has been observation of two main anaplerotic pathways that are governed by enzymic activities able to fix CO 2 to organic molecules. These pathways are involved in amino acid and pyrimidine synthesis, and are governed by phosphoenolpyruvate carboxylase (PpC) and carbamoyl-phosphate synthase (CpS), which catalyse the fixation of CO 2 to phosphoenolpyruvate and glutamine, respectively (Fig.…”

Section: Introductionmentioning

confidence: 99%

The relevance of carbon dioxide metabolism in Streptococcus thermophilus

Arioli¹,

Roncada

Salzano

et al. 2009

Microbiology

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Streptococcus thermophilus is a major component of dairy starter cultures used for the manufacture of yoghurt and cheese. In this study, the CO 2 metabolism of S. thermophilus DSM 20617 T , grown in either a N 2 atmosphere or an enriched CO 2 atmosphere, was analysed using both genetic and proteomic approaches. Growth experiments performed in a chemically defined medium revealed that CO 2 depletion resulted in bacterial arginine, aspartate and uracil auxotrophy. Moreover, CO 2 depletion governed a significant change in cell morphology, and a high reduction in biomass production. A comparative proteomic analysis revealed that cells of S. thermophilus showed a different degree of energy status depending on the CO 2 availability. In agreement with proteomic data, cells grown under N 2 showed a significantly higher milk acidification rate compared with those grown in an enriched CO 2 atmosphere. Experiments carried out on S. thermophilus wild-type and its derivative mutant, which was inactivated in the phosphoenolpyruvate carboxylase and carbamoyl-phosphate synthase activities responsible for fixing CO 2 to organic molecules, suggested that the anaplerotic reactions governed by these enzymes have a central role in bacterial metabolism. Our results reveal the capnophilic nature of this micro-organism, underlining the essential role of CO 2 in S. thermophilus physiology, and suggesting potential applications in dairy fermentation processes.

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Complete sequence and comparative genome analysis of the dairy bacterium Streptococcus thermophilus

Cited by 454 publications

References 31 publications

The complete genome sequence ofLactobacillus bulgaricusreveals extensive and ongoing reductive evolution

The complete genome sequence ofLactobacillus bulgaricusreveals extensive and ongoing reductive evolution

CRISPR-based screening of genomic island excision events in bacteria

The relevance of carbon dioxide metabolism in Streptococcus thermophilus

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