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Transcriptomes reveal genetic signatures underlying physiological variations imposed by different fermentation conditions in Lactobacillus plantarum.

ABSTRACT: Lactic acid bacteria (LAB) are utilized widely for the fermentation of foods. In the current post-genomic era, tools have been developed that explore genetic diversity among LAB strains aiming to link these variations to differential phenotypes observed in the strains investigated. However, these genotype-phenotype matching approaches fail to assess the role of conserved genes in the determination of physiological characteristics of cultures by environmental conditions. This manuscript describes a complementary approach in which Lactobacillus plantarum WCFS1 was fermented under a variety of conditions that differ in temperature, pH, as well as NaCl, amino acid, and O(2) levels. Samples derived from these fermentations were analyzed by full-genome transcriptomics, paralleled by the assessment of physiological characteristics, e.g., maximum growth rate, yield, and organic acid profiles. A data-storage and -mining suite designated FermDB was constructed and exploited to identify correlations between fermentation conditions and industrially relevant physiological characteristics of L. plantarum, as well as the associated transcriptome signatures. Finally, integration of the specific fermentation variables with the transcriptomes enabled the reconstruction of the gene-regulatory networks involved. The fermentation-genomics platform presented here is a valuable complementary approach to earlier described genotype-phenotype matching strategies which allows the identification of transcriptome signatures underlying physiological variations imposed by different fermentation conditions.

SUBMITTER: Bron PA

PROVIDER: S-EPMC3389018 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Transcriptomes reveal genetic signatures underlying physiological variations imposed by different fermentation conditions in Lactobacillus plantarum.

Bron Peter A PA Wels Michiel M Bongers Roger S RS van Bokhorst-van de Veen Hermien H Wiersma Anne A Overmars Lex L Marco Maria L ML Kleerebezem Michiel M

PloS one 20120703 7

Lactic acid bacteria (LAB) are utilized widely for the fermentation of foods. In the current post-genomic era, tools have been developed that explore genetic diversity among LAB strains aiming to link these variations to differential phenotypes observed in the strains investigated. However, these genotype-phenotype matching approaches fail to assess the role of conserved genes in the determination of physiological characteristics of cultures by environmental conditions. This manuscript describes ...[more]

PMID: 22802930

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Project description:BACKGROUND: Lactic acid bacteria (LAB) are applied worldwide in the production of a variety of fermented food products. Additionally, specific Lactobacillus species are nowadays recognized for their health-promoting effects on the consumer. To optimally exert such beneficial effects, it is considered of great importance that these probiotic bacteria reach their target sites in the gut alive. METHODOLOGY/PRINCIPAL FINDINGS: In the accompanying manuscript by Bron et al. the probiotic model organism Lactobacillus plantarum WCFS1 was cultured under different fermentation conditions, which was complemented by the determination of the corresponding molecular responses by full-genome transcriptome analyses. Here, the gastrointestinal (GI) survival of the cultures produced was assessed in an in vitro assay. Variations in fermentation conditions led to dramatic differences in GI-tract survival (up to 7-log) and high robustness could be associated with low salt and low pH during the fermentations. Moreover, random forest correlation analyses allowed the identification of specific transcripts associated with robustness. Subsequently, the corresponding genes were targeted by genetic engineering, aiming to enhance robustness, which could be achieved for 3 of the genes that negatively correlated with robustness and where deletion derivatives displayed enhanced survival compared to the parental strain. Specifically, a role in GI-tract survival could be confirmed for the lp_1669-encoded AraC-family transcription regulator, involved in capsular polysaccharide remodeling, the penicillin-binding protein Pbp2A involved in peptidoglycan biosynthesis, and the Na(+)/H(+) antiporter NapA3. Moreover, additional physiological analysis established a role for Pbp2A and NapA3 in bile salt and salt tolerance, respectively. CONCLUSION: Transcriptome trait matching enabled the identification of biomarkers for bacterial (gut-)robustness, which is important for our molecular understanding of GI-tract survival and could facilitate the design of culture conditions aimed to enhance probiotic culture robustness.

Project description:Strains of Lactobacillus plantarum were grown and stored in cherry (ChJ), pineapple (PJ), carrot (CJ), and tomato (TJ) juices to mimic the chemical composition of the respective matrices. Wheat flour hydrolysate (WFH), whey milk (W), and MRS broth were also used as representatives of other ecosystems. The growth rates and cell densities of L. plantarum strains during fermentation (24 h at 30°C) and storage (21 days at 4°C) differed only in part, being mainly influenced by the matrix. ChJ and PJ were the most stressful juices for growth and survival. Overall, the growth in juices was negatively correlated with the initial concentration of malic acid and carbohydrates. The consumption of malic acid was noticeable for all juices, but mainly during fermentation and storage of ChJ. Decreases of branched-chain amino acids (BCAA)-with the concomitant increase of their respective branched alcohols-and His and increases of Glu and gamma-aminobutyric acid (GABA) were the main traits of the catabolism of free amino acids (FAA), which were mainly evident under less acidic conditions (CJ and TJ). The increase of Tyr was found only during storage of ChJ. Some aldehydes (e.g., 3-methyl-butanal) were reduced to the corresponding alcohols (e.g., 3-methyl-1-butanol). After both fermentation and storage, acetic acid increased in all fermented juices, which implied the activation of the acetate kinase route. Diacetyl was the ketone found at the highest level, and butyric acid increased in almost all fermented juices. Data were processed through multidimensional statistical analyses. Except for CJ, the juices (mainly ChJ) seemed to induce specific metabolic traits, which differed in part among the strains. This study provided more in-depth knowledge on the metabolic mechanisms of growth and maintenance of L. plantarum in vegetable and fruit habitats, which also provided helpful information to select the most suitable starters for fermentation of targeted matrices.

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Transcriptomes reveal genetic signatures underlying physiological variations imposed by different fermentation conditions in Lactobacillus plantarum.

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Transcriptomes reveal genetic signatures underlying physiological variations imposed by different fermentation conditions in Lactobacillus plantarum.

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