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Transcriptome signatures of class I and III stress response deregulation in Lactobacillus plantarum reveal pleiotropic adaptation.

ABSTRACT: BACKGROUND: To cope with environmental challenges bacteria possess sophisticated defense mechanisms that involve stress-induced adaptive responses. The canonical stress regulators CtsR and HrcA play a central role in the adaptations to a plethora of stresses in a variety of organisms. Here, we determined the CtsR and HrcA regulons of the lactic acid bacterium Lactobacillus plantarum WCFS1 grown under reference (28°C) and elevated (40°C) temperatures, using ctsR, hrcA, and ctsR-hrcA deletion mutants. RESULTS: While the maximum specific growth rates of the mutants and the parental strain were similar at both temperatures (0.33?±?0.02 h(-1) and 0.34?±?0.03 h(-1), respectively), DNA microarray analyses revealed that the CtsR or HrcA deficient strains displayed altered transcription patterns of genes encoding functions involved in transport and binding of sugars and other compounds, primary metabolism, transcription regulation, capsular polysaccharide biosynthesis, as well as fatty acid metabolism. These transcriptional signatures enabled the refinement of the gene repertoire that is directly or indirectly controlled by CtsR and HrcA of L. plantarum. Deletion of both regulators, elicited transcriptional changes of a large variety of additional genes in a temperature-dependent manner, including genes encoding functions involved in cell-envelope remodeling. Moreover, phenotypic assays revealed that both transcription regulators contribute to regulation of resistance to hydrogen peroxide stress. The integration of these results allowed the reconstruction of CtsR and HrcA regulatory networks in L. plantarum, highlighting the significant intertwinement of class I and III stress regulons. CONCLUSIONS: Taken together, our results enabled the refinement of the CtsR and HrcA regulatory networks in L. plantarum, illustrating the complex nature of adaptive stress responses in this bacterium.

SUBMITTER: Van Bokhorst-van de Veen H

PROVIDER: S-EPMC3842655 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Transcriptome signatures of class I and III stress response deregulation in Lactobacillus plantarum reveal pleiotropic adaptation.

Van Bokhorst-van de Veen Hermien H Bongers Roger S RS Wels Michiel M Bron Peter A PA Kleerebezem Michiel M

Microbial cell factories 20131118

<h4>Background</h4>To cope with environmental challenges bacteria possess sophisticated defense mechanisms that involve stress-induced adaptive responses. The canonical stress regulators CtsR and HrcA play a central role in the adaptations to a plethora of stresses in a variety of organisms. Here, we determined the CtsR and HrcA regulons of the lactic acid bacterium Lactobacillus plantarum WCFS1 grown under reference (28°C) and elevated (40°C) temperatures, using ctsR, hrcA, and ctsR-hrcA deleti ...[more]

PMID: 24238744

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Project description:The widespread use of antibiotics has caused great concern in the biosafety of probiotics. In this study, we conducted a 12-month adaptive laboratory evolution (ALE) experiment to select for antibiotics-adapted Lactobacillus plantarum P-8, a dairy-originated probiotic bacterium. During the ALE process, the ampicillin MIC for the parental L. plantarum P-8 strain increased gradually and reached the maximum level of bacterial fitness. To elucidate the molecular mechanisms underlying the ampicillin-resistant phenotype, we comparatively analyzed the genomes and proteomes of the parental strain (L. plantarum P-8) and two adapted lines (L. plantarum 400g and L. plantarum 1600g). The adapted lines showed alterations in their carbon, amino acid, and cell surface-associated metabolic pathways. Then, gene disruption mutants were created to determine the role of six highly expressed genes in contributing to the enhanced ampicillin resistance. Inactivation of an ATP-dependent Clp protease/the ATP-binding subunit ClpL, a small heat shock protein, or a hypothetical protein resulted in partial but significant phenotypic reversion, confirming their necessary roles in the bacterial adaptation to ampicillin. Genomic analysis confirmed that none of the ampicillin-specific differential expressed genes were flanked by any mobile genetic elements; thus, even though long-term exposure to ampicillin upregulated their expression, there is low risk of spread of these genes and adapted drug resistance to other bacteria via horizontal gene transfer. Our study has provided evidence of the biosafety of probiotics even when used in the presence of antibiotics.IMPORTANCE Antibiotic resistance acquired by adaptation to certain antibiotics has led to growing public concerns. Here, a long-term evolution experiment was used together with proteomic analysis to identify genes/proteins responsible for the adaptive phenotype. This work has provided novel insights into the biosafety of new probiotics with high tolerance to antibiotics.

Project description:A triathlon is an extremely high-intensity exercise and a challenge for physiological adaptation. A triathlete's microbiome might be modulated by diet, age, medical treatments, lifestyle, and exercise, thereby maintaining aerobiosis and optimum health and performance. Probiotics, prebiotics, and synbiotics have been reported to have health-promoting activities (e.g., immunoregulation and cancer prevention). However, few studies have addressed how probiotics affect the microbiota of athletes and how this translates into functional activities. In our previous study, we found that Lactobacillus plantarum PS128 could ameliorate inflammation and oxidative stress, with improved exercise performance. Thus, here we investigate how the microbiota of triathletes are altered by L. plantarum PS128 supplementation, not only for exercise performance but also for possible physiological adaptation. The triathletes were assigned to two groups: an L. plantarum 128 supplement group (LG, 3 × 1010 colony-forming units (CFU)/day) and a placebo group (PG). Both groups continued with their regular exercise training for the next 4 weeks. The endurance performance, body composition, biochemistries, blood cells, microbiota, and associated metabolites were further investigated. PS128 significantly increased the athletes' endurance, by about 130% as compared to the PG group, but there was no significant difference in maximal oxygen consumption (VO2max) and composition between groups. The PS128 supplementation (LG) modulated the athlete's microbiota with both significant decreases (Anaerotruncus, Caproiciproducens, Coprobacillus, Desulfovibrio, Dielma, Family_XIII, Holdemania, and Oxalobacter) and increases (Akkermansia, Bifidobacterium, Butyricimonas, and Lactobacillus), and the LG showed lower diversity when compared to the PG. Also, the short-chain fatty acids (SCFAs; acetate, propionate, and butyrate) of the LG were significantly higher than the PG, which might be a result of a modulation of the associated microbiota. In conclusion, PS128 supplementation was associated with an improvement on endurance running performance through microbiota modulation and related metabolites, but not in maximal oxygen uptake.

Dataset Information

Transcriptome signatures of class I and III stress response deregulation in Lactobacillus plantarum reveal pleiotropic adaptation.

Publications

Transcriptome signatures of class I and III stress response deregulation in Lactobacillus plantarum reveal pleiotropic adaptation.

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