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Characterization of transcriptional response of Lactobacillus plantarum under acidic conditions provides insight into bacterial adaptation in fermentative environments.

ABSTRACT: Lactic acid bacteria (LAB) play an important role in kimchi fermentation by metabolizing raw materials into diverse metabolites. Bacterial adaptation is therefore a crucial element of fermentation. In this study, we investigated the transcriptional changes of Lactobacillus plantarum under acidic conditions to evaluate the elements of bacterial adaptation critical for fermentation. Differentially expressed genes (DEGs) have shown that transport function is primarily affected by acidic conditions. Five of the 13 significantly down-regulated genes and 7 of the 25 significantly up-regulated genes were found to have transport-related functions. We quantified the intracellular leucine content of bacteria grown at different pH ranges, determining that optimal bacterial leucine transport could be controlled by acidity during fermentation. Inhibition of L. plantarum growth was investigated and compared with other LAB at a pH range of 6.2-5.0. Interestingly, valinomycin inhibited L. plantarum growth from pH 6.2 to 5.0. This showed that L. plantarum had a wider range of transport functions than other LAB. These results suggested that L. plantarum had robust transport functions, and that this was the crucial factor for bacterial adaptation during fermentation.

SUBMITTER: Jung S

PROVIDER: S-EPMC7645587 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Characterization of transcriptional response of Lactobacillus plantarum under acidic conditions provides insight into bacterial adaptation in fermentative environments.

Jung Sera S Lee Jong-Hee JH

Scientific reports 20201105 1

Lactic acid bacteria (LAB) play an important role in kimchi fermentation by metabolizing raw materials into diverse metabolites. Bacterial adaptation is therefore a crucial element of fermentation. In this study, we investigated the transcriptional changes of Lactobacillus plantarum under acidic conditions to evaluate the elements of bacterial adaptation critical for fermentation. Differentially expressed genes (DEGs) have shown that transport function is primarily affected by acidic conditions. ...[more]

PMID: 33154427

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Project description:In the past decade, the sequencing of large cohorts of Saccharomyces cerevisiae strains has revealed a landscape of genomic regions acquired by Horizontal Gene Transfer (HGT). The genes acquired by HGT play important roles in yeast adaptation to the fermentation process, improving nitrogen and carbon source utilization. However, the functional characterization of these genes at the molecular level has been poorly attended. In this work, we carried out a systematic analysis of the promoter activity and protein level of 30 genes contained in three horizontally acquired regions commonly known as regions A, B, and C. In three strains (one for each region), we used the luciferase reporter gene and the mCherry fluorescent protein to quantify the transcriptional and translational activity of these genes, respectively. We assayed the strains generated in four different culture conditions; all showed low levels of transcriptional and translational activity across these environments. However, we observed an increase in protein levels under low nitrogen culture conditions, suggesting a possible role of the horizontally acquired genes in the adaptation to nitrogen-limited environments. Furthermore, since the strains carrying the luciferase reporter gene are null mutants for the horizontally acquired genes, we assayed growth parameters (latency time, growth rate, and efficiency) and the fermentation kinetics in this set of deletion strains. The results showed that single deletion of 20 horizontally acquired genes modified the growth parameters, whereas the deletion of five of them altered the maximal CO2 production rate (Vmax). Interestingly, we observed a correlation between growth parameters and Vmax for an ORF within region A, encoding an ortholog to a thiamine (vitamin B1) transporter whose deletion decreased the growth rate, growth efficiency, and CO2 production. Altogether, our results provided molecular and phenotypic evidence highlighting the importance of horizontally acquired genes in yeast adaptation to fermentative environments.

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.

Dataset Information

Characterization of transcriptional response of Lactobacillus plantarum under acidic conditions provides insight into bacterial adaptation in fermentative environments.

Publications

Characterization of transcriptional response of Lactobacillus plantarum under acidic conditions provides insight into bacterial adaptation in fermentative environments.

Similar Datasets

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