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Cited by 17Probiotics and Fermented FoodsBacterial Genetics and BiotechnologyMicrobial Metabolic Engineering and Bioproduction

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Effects of pH and Osmotic Changes on the Metabolic Expressions of Bacillus subtilis Strain 168 in Metabolite Pathways including Leucine Metabolism

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Park, Min-Kyung, Lee, Soyeon, Kim, Young-Suk·2022·Metabolites
DOI 10.3390/metabo12020112PMC PMC8880083
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Abstract

Bacillus subtilis is often exposed to diverse culture conditions with the aim of improving hygiene or food quality. This can lead to changes in the volatile metabolite profiles related to the quality of fermented foods. To comprehensively interpret the associated metabolic expressions, changes in intracellular primary and extracellular secondary volatile metabolites were investigated by exposing B. subtilis to an alkaline pH (BP, pH 8.0) and a high salt concentration (BS, 1 M). In particular, B. subtilis was cultured in a leucine-enriched medium to investigate the formation of leucine-derived volatile metabolites. This study observed metabolic changes in several metabolic pathways, including carbohydrate metabolism, amino acid metabolism, fatty acid metabolism, and leucine degradation. The formation of proline (an osmolyte), furans, pyrrole, and monosaccharide sugars (glucose, galactose, and fructose) was enhanced in BS, whereas fatty acid derivatives (ketones and alcohols) increased in BP. In the case of leucine degradation, 3-methyl-butanal and 3-methylbutanol could be salt-specific metabolites, while the contents of 3-methylbutanoic acid and 3-methylbutylacetate increased in BP. These results show culture condition-specific metabolic changes, especially secondary volatile metabolites related to the sensory property of foods, in B. subtilis.

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Figure 1 OPLS-DA score scatter plot of control (BC), alkaline pH (BP), and high salt concentration (BS) groups based on primary metabolite profiles (A) and secondary volatile metabolite profiles (B) obtained according to culture times. Permutation test plots based on primary metabolites (C) and secondary volatile metabolites (D) were conducted. Colors represent the following: red-BS, blue-BP, and green-BC. The meaning of the letters and numbers inside the score plot are the following: BC11-13, 21-23, and 31-33 (control samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively), BP11-13, 21-23, and 31-33 (BP samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively), and BS11-13, 21-23, and 31-33 (BS samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively).
Figure 1 OPLS-DA score scatter plot of control (BC), alkaline pH (BP), and high salt concentration (BS) groups based on primary metabolite profiles (A) and secondary volatile metabolite profiles (B) obtained according to culture times. Permutation test plots based on primary metabolites (C) and secondary volatile metabolites (D) were conducted. Colors represent the following: red-BS, blue-BP, and green-BC. The meaning of the letters and numbers inside the score plot are the following: BC11-13, 21-23, and 31-33 (control samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively), BP11-13, 21-23, and 31-33 (BP samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively), and BS11-13, 21-23, and 31-33 (BS samples obtained at phases Ⅰ, Ⅱ, and Ⅲ in replication, respectively).CC BY · PubMed Central
Figure 2 The heatmap shows the z-score value of each metabolite selected by VIP score and pcorr values (VIP > 1 and ΙpcorrΙ > 0.5) of the OPLS-DA model, and color intensity represents the metabolic expressions: red represents the up-expression and blue the down-expression. Main metabolism was divided into three parts: C: carbohydrate metabolism, A: amino acid metabolism, and F: fatty acid metabolism. Abbreviations are as follows: BC: control sample, BP: cultivation under alkaline pH (pH 8.0), BS: cultivation under high salt concentration (1 M salt concentration), Ⅰ: exponential time (phase Ⅰ), Ⅱ: early stationary time (phase Ⅱ), and Ⅲ: later stationary time (phase Ⅲ). Boxes in each phase (Ⅰ, Ⅱ, and Ⅲ) represent replicas of the measurements.
Figure 2 The heatmap shows the z-score value of each metabolite selected by VIP score and pcorr values (VIP > 1 and ΙpcorrΙ > 0.5) of the OPLS-DA model, and color intensity represents the metabolic expressions: red represents the up-expression and blue the down-expression. Main metabolism was divided into three parts: C: carbohydrate metabolism, A: amino acid metabolism, and F: fatty acid metabolism. Abbreviations are as follows: BC: control sample, BP: cultivation under alkaline pH (pH 8.0), BS: cultivation under high salt concentration (1 M salt concentration), Ⅰ: exponential time (phase Ⅰ), Ⅱ: early stationary time (phase Ⅱ), and Ⅲ: later stationary time (phase Ⅲ). Boxes in each phase (Ⅰ, Ⅱ, and Ⅲ) represent replicas of the measurements.CC BY · PubMed Central
Figure 3 The possible metabolic pathways of specific metabolites obtained at phase Ⅲ in B. subtilis. The fold changes (>1.5) compared to BC were visualized by heatmaps. Metabolites showing significant changes compared to the control are written in red letters. Up-expressed metabolites are represented by a red color, while down-expressed metabolites are shown in a blue color. Abbreviations are as follows: BP: alkaline pH; BS: high salt concentration; Glu: glutamic acid; Gln: glutamine; Pro: proline; Asp: aspartic acid; Orn: ornithine; Lys: lysine; Fum: fumaric acid; Mal: malic acid; SA: succinic acid; Val: valine, Phe: phenylalanine; Leu: leucine.
Figure 3 The possible metabolic pathways of specific metabolites obtained at phase Ⅲ in B. subtilis. The fold changes (>1.5) compared to BC were visualized by heatmaps. Metabolites showing significant changes compared to the control are written in red letters. Up-expressed metabolites are represented by a red color, while down-expressed metabolites are shown in a blue color. Abbreviations are as follows: BP: alkaline pH; BS: high salt concentration; Glu: glutamic acid; Gln: glutamine; Pro: proline; Asp: aspartic acid; Orn: ornithine; Lys: lysine; Fum: fumaric acid; Mal: malic acid; SA: succinic acid; Val: valine, Phe: phenylalanine; Leu: leucine.CC BY · PubMed Central
Figure 4 Leucine degradation pathway, reflecting the metabolite changes obtained at phases Ⅰ–Ⅲ in B. subtilis under different cultivation conditions (BC: control; BP: alkaline pH; BS: high salt concentration). The colors (green and orange) represent the changes of metabolites according to culture times in each condition. Blue and red colors represent the metabolic response to culture conditions.
Figure 4 Leucine degradation pathway, reflecting the metabolite changes obtained at phases Ⅰ–Ⅲ in B. subtilis under different cultivation conditions (BC: control; BP: alkaline pH; BS: high salt concentration). The colors (green and orange) represent the changes of metabolites according to culture times in each condition. Blue and red colors represent the metabolic response to culture conditions.CC BY · PubMed Central

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Metadata

Authors
Park, M.-K., Lee, S., & Kim, Y.-S.
Affiliations
  • Ewha Womans University (KR)
  • Department of Food Science and Biotechnology, Ewha Womans University, Seoul 03760, Korea
Corresponding author
Kim, Young-Suk
ORCID
Venue
Metabolites
Publisher
MDPI AG
Published
2022-01-25
Volume
12
Issue
2
Pages
112
ISSN
2218-1989 (ISSN-L)
DOI
10.3390/metabo12020112
PMC
PMC8880083
OpenAlex
W4210345244
Cited by
15
References
39
Citations by year
2026: 6 · 2025: 4 · 2024: 1 · 2023: 3 · 2022: 1
FWCI
1.20
Type
journal article
Language
en
Open access
Licence
Locations
  • Metabolites (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Research Foundation of Korea (NRF-2020R1A2C2004724)
  • Korea government (BK 21 FOUR) (No. 4299990914600)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
Keywords
Bacillus subtilis, pH stress, osmotic stress, high salt concentration, alkaline pH, leucine metabolism, leucine degradation, volatile metabolites, secondary metabolites, proline, furan, pyrrole, fatty acid derivatives, isovaleric acid, isoamyl alcohol, 3-methylbutanal, fermented food quality, sensory properties

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