Comparative physiological and transcriptomic analysis of sono-biochemical control over post-acidification of Lactobacillus delbrueckii subsp. bulgaricus

Thermosonication (UT) prestress treatments combining with varied fermentation patterns has been revealed as an effective method to regulate post-acidification as exerted by Lactobacillus delbrueckii subsp. bulgaricus (L. delbrueckii), but sono-biochemical controlling mechanisms remain elusive. This...

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Veröffentlicht in:Food microbiology 2024-09, Vol.122, p.104563-104563, Article 104563
Hauptverfasser: Zhang, Xiaohui, Zheng, Yuanrong, Zhou, Changyu, Cao, Jinxuan, Pan, Daodong, Cai, Zhendong, Wu, Zhen, Xia, Qiang
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Cao, Jinxuan
Pan, Daodong
Cai, Zhendong
Wu, Zhen
Xia, Qiang
description Thermosonication (UT) prestress treatments combining with varied fermentation patterns has been revealed as an effective method to regulate post-acidification as exerted by Lactobacillus delbrueckii subsp. bulgaricus (L. delbrueckii), but sono-biochemical controlling mechanisms remain elusive. This study employed physiological and transcriptomic analysis to explore the response mechanism of L. delbrueckii to UT-induced microstress (600 W, 33 kHz, 10 min). UT stress-induced inhibition of acidification of L. delbrueckii during (post)-fermentation was first confirmed, relying on the UT process parameters such as stress exposure duration and UT power. The significantly enhanced membrane permeability in cells treated by 600 W for 10 min than the microbes stressed by 420 W for 20 min suggested the higher dependence of UT-derived stresses on the treatment durations, relative to the ultrasonic powers. In addition, ultrasonication treatment-induced changes in cell membrane integrity enhanced and/or disrupted permeability of L. delbrueckii, resulting in an imbalance in intracellular conditions associated with corresponding alterations in metabolic behaviors and fermentation efficiencies. UT-prestressed inoculum exhibited a 21.46% decrease in the membrane potential during the lag phase compared to untreated samples, with an intracellular pH of 5.68 ± 0.12, attributed to the lower activities of H+-ATPase and lactate dehydrogenase due to UT stress pretreatments. Comparative transcriptomic analysis revealed that UT prestress influenced the genes related to glycolysis, pyruvate metabolism, fatty acid synthesis, and ABC transport. The genes encoding 3-oxoacyl-[acyl-carrier-protein] reductases I, II, and III, CoA carboxylase, lactate dehydrogenase, pyruvate oxidase, glucose-6-phosphate isomerase, and glycerol-3-phosphate dehydrogenase were downregulated, thus identifying the relevance of the UT microstresses-downregulated absorption and utilization of carbohydrates with the attenuated fatty acid production and energy metabolisms. These findings could contribute to provide a better understanding of the inactivated effects on the post-acidification of L. delbrueckii by ultrasonic pretreatments, thus providing theoretical basis for the targeted optimization of acidification inhibition efficiencies for yogurt products during chilled preservation processes. [Display omitted] •Sono-biochemical effect as elucidated by physiological and transcriptomic analysis.•Ultrasound microstr
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This study employed physiological and transcriptomic analysis to explore the response mechanism of L. delbrueckii to UT-induced microstress (600 W, 33 kHz, 10 min). UT stress-induced inhibition of acidification of L. delbrueckii during (post)-fermentation was first confirmed, relying on the UT process parameters such as stress exposure duration and UT power. The significantly enhanced membrane permeability in cells treated by 600 W for 10 min than the microbes stressed by 420 W for 20 min suggested the higher dependence of UT-derived stresses on the treatment durations, relative to the ultrasonic powers. In addition, ultrasonication treatment-induced changes in cell membrane integrity enhanced and/or disrupted permeability of L. delbrueckii, resulting in an imbalance in intracellular conditions associated with corresponding alterations in metabolic behaviors and fermentation efficiencies. UT-prestressed inoculum exhibited a 21.46% decrease in the membrane potential during the lag phase compared to untreated samples, with an intracellular pH of 5.68 ± 0.12, attributed to the lower activities of H+-ATPase and lactate dehydrogenase due to UT stress pretreatments. Comparative transcriptomic analysis revealed that UT prestress influenced the genes related to glycolysis, pyruvate metabolism, fatty acid synthesis, and ABC transport. The genes encoding 3-oxoacyl-[acyl-carrier-protein] reductases I, II, and III, CoA carboxylase, lactate dehydrogenase, pyruvate oxidase, glucose-6-phosphate isomerase, and glycerol-3-phosphate dehydrogenase were downregulated, thus identifying the relevance of the UT microstresses-downregulated absorption and utilization of carbohydrates with the attenuated fatty acid production and energy metabolisms. These findings could contribute to provide a better understanding of the inactivated effects on the post-acidification of L. delbrueckii by ultrasonic pretreatments, thus providing theoretical basis for the targeted optimization of acidification inhibition efficiencies for yogurt products during chilled preservation processes. [Display omitted] •Sono-biochemical effect as elucidated by physiological and transcriptomic analysis.•Ultrasound microstress led to weakened energy metabolism during post-fermentation.•Inhibited acidification related to UT-induced in energy metabolism and nutrient transport.•Ultrasound microstress reduced activities of H+-ATPase and lactate dehydrogenase.•UT stress evidenced by microstructure characterization of UT-stressed L. 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All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c336t-78ea035eb499fb0aa26e5b29b1f1363c8ced1f350840a4b978f4aa03dcd8d2ab3</cites><orcidid>0000-0003-4426-852X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.fm.2024.104563$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38839237$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Xiaohui</creatorcontrib><creatorcontrib>Zheng, Yuanrong</creatorcontrib><creatorcontrib>Zhou, Changyu</creatorcontrib><creatorcontrib>Cao, Jinxuan</creatorcontrib><creatorcontrib>Pan, Daodong</creatorcontrib><creatorcontrib>Cai, Zhendong</creatorcontrib><creatorcontrib>Wu, Zhen</creatorcontrib><creatorcontrib>Xia, Qiang</creatorcontrib><title>Comparative physiological and transcriptomic analysis of sono-biochemical control over post-acidification of Lactobacillus delbrueckii subsp. bulgaricus</title><title>Food microbiology</title><addtitle>Food Microbiol</addtitle><description>Thermosonication (UT) prestress treatments combining with varied fermentation patterns has been revealed as an effective method to regulate post-acidification as exerted by Lactobacillus delbrueckii subsp. bulgaricus (L. delbrueckii), but sono-biochemical controlling mechanisms remain elusive. This study employed physiological and transcriptomic analysis to explore the response mechanism of L. delbrueckii to UT-induced microstress (600 W, 33 kHz, 10 min). UT stress-induced inhibition of acidification of L. delbrueckii during (post)-fermentation was first confirmed, relying on the UT process parameters such as stress exposure duration and UT power. The significantly enhanced membrane permeability in cells treated by 600 W for 10 min than the microbes stressed by 420 W for 20 min suggested the higher dependence of UT-derived stresses on the treatment durations, relative to the ultrasonic powers. In addition, ultrasonication treatment-induced changes in cell membrane integrity enhanced and/or disrupted permeability of L. delbrueckii, resulting in an imbalance in intracellular conditions associated with corresponding alterations in metabolic behaviors and fermentation efficiencies. UT-prestressed inoculum exhibited a 21.46% decrease in the membrane potential during the lag phase compared to untreated samples, with an intracellular pH of 5.68 ± 0.12, attributed to the lower activities of H+-ATPase and lactate dehydrogenase due to UT stress pretreatments. Comparative transcriptomic analysis revealed that UT prestress influenced the genes related to glycolysis, pyruvate metabolism, fatty acid synthesis, and ABC transport. The genes encoding 3-oxoacyl-[acyl-carrier-protein] reductases I, II, and III, CoA carboxylase, lactate dehydrogenase, pyruvate oxidase, glucose-6-phosphate isomerase, and glycerol-3-phosphate dehydrogenase were downregulated, thus identifying the relevance of the UT microstresses-downregulated absorption and utilization of carbohydrates with the attenuated fatty acid production and energy metabolisms. These findings could contribute to provide a better understanding of the inactivated effects on the post-acidification of L. delbrueckii by ultrasonic pretreatments, thus providing theoretical basis for the targeted optimization of acidification inhibition efficiencies for yogurt products during chilled preservation processes. [Display omitted] •Sono-biochemical effect as elucidated by physiological and transcriptomic analysis.•Ultrasound microstress led to weakened energy metabolism during post-fermentation.•Inhibited acidification related to UT-induced in energy metabolism and nutrient transport.•Ultrasound microstress reduced activities of H+-ATPase and lactate dehydrogenase.•UT stress evidenced by microstructure characterization of UT-stressed L. Bulgaricus.</description><subject>absorption</subject><subject>acidification</subject><subject>acyl carrier protein</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>energy</subject><subject>exposure duration</subject><subject>fatty acids</subject><subject>Fermentation</subject><subject>food microbiology</subject><subject>Gene Expression Profiling</subject><subject>glucose-6-phosphate isomerase</subject><subject>glycerol-3-phosphate dehydrogenase</subject><subject>glycolysis</subject><subject>Hydrogen-Ion Concentration</subject><subject>inoculum</subject><subject>lactate dehydrogenase</subject><subject>Lactic acid bacteria</subject><subject>Lactobacillus delbrueckii - genetics</subject><subject>Lactobacillus delbrueckii - metabolism</subject><subject>membrane permeability</subject><subject>membrane potential</subject><subject>Post-fermentation acidification</subject><subject>pyruvate oxidase</subject><subject>pyruvic acid</subject><subject>Sonication</subject><subject>Sono-biochemical control</subject><subject>Transcriptome</subject><subject>Transcriptomic analysis</subject><subject>transcriptomics</subject><subject>ultrasonic treatment</subject><subject>ultrasonics</subject><subject>yogurt</subject><issn>0740-0020</issn><issn>1095-9998</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkT-P1DAQxS0E4paDngq5pMkyjhNvTIdW_DlpJRqoLdsZ33lx4mA7K9034ePiZQ86dNVoZn7vSTOPkNcMtgyYeHfcumnbQtvVtusFf0I2DGTfSCmHp2QDuw4agBauyIucjwCM9Vw-J1d8GLhs-W5Dfu3jtOikiz8hXe7us48h3nqrA9XzSEvSc7bJLyVO3taRDhXJNDqa4xwb46O9w-kPb-NcUgw0njDRJebSaOtH7-qy-DifNQdtSzR1HMKa6YjBpBXtD-9pXk1ettSs4VYnb9f8kjxzOmR89VCvyfdPH7_tvzSHr59v9h8OjeVclGY3oAbeo-mkdAa0bgX2ppWGOcYFt4PFkTnew9CB7ozcDa7TVTHacRhbbfg1eXvxXVL8uWIuavLZYgh6xrhmxevLBBMg2eMoiL7dCTG0FYULalPMOaFTS_KTTveKgTpHp47KTeocnbpEVyVvHtxXM-H4T_A3qwq8vwBY33HymFS2Hud6oE9oixqj_7_7b5E2rS4</recordid><startdate>20240901</startdate><enddate>20240901</enddate><creator>Zhang, Xiaohui</creator><creator>Zheng, Yuanrong</creator><creator>Zhou, Changyu</creator><creator>Cao, Jinxuan</creator><creator>Pan, Daodong</creator><creator>Cai, Zhendong</creator><creator>Wu, Zhen</creator><creator>Xia, Qiang</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0003-4426-852X</orcidid></search><sort><creationdate>20240901</creationdate><title>Comparative physiological and transcriptomic analysis of sono-biochemical control over post-acidification of Lactobacillus delbrueckii subsp. bulgaricus</title><author>Zhang, Xiaohui ; 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This study employed physiological and transcriptomic analysis to explore the response mechanism of L. delbrueckii to UT-induced microstress (600 W, 33 kHz, 10 min). UT stress-induced inhibition of acidification of L. delbrueckii during (post)-fermentation was first confirmed, relying on the UT process parameters such as stress exposure duration and UT power. The significantly enhanced membrane permeability in cells treated by 600 W for 10 min than the microbes stressed by 420 W for 20 min suggested the higher dependence of UT-derived stresses on the treatment durations, relative to the ultrasonic powers. In addition, ultrasonication treatment-induced changes in cell membrane integrity enhanced and/or disrupted permeability of L. delbrueckii, resulting in an imbalance in intracellular conditions associated with corresponding alterations in metabolic behaviors and fermentation efficiencies. UT-prestressed inoculum exhibited a 21.46% decrease in the membrane potential during the lag phase compared to untreated samples, with an intracellular pH of 5.68 ± 0.12, attributed to the lower activities of H+-ATPase and lactate dehydrogenase due to UT stress pretreatments. Comparative transcriptomic analysis revealed that UT prestress influenced the genes related to glycolysis, pyruvate metabolism, fatty acid synthesis, and ABC transport. The genes encoding 3-oxoacyl-[acyl-carrier-protein] reductases I, II, and III, CoA carboxylase, lactate dehydrogenase, pyruvate oxidase, glucose-6-phosphate isomerase, and glycerol-3-phosphate dehydrogenase were downregulated, thus identifying the relevance of the UT microstresses-downregulated absorption and utilization of carbohydrates with the attenuated fatty acid production and energy metabolisms. These findings could contribute to provide a better understanding of the inactivated effects on the post-acidification of L. delbrueckii by ultrasonic pretreatments, thus providing theoretical basis for the targeted optimization of acidification inhibition efficiencies for yogurt products during chilled preservation processes. [Display omitted] •Sono-biochemical effect as elucidated by physiological and transcriptomic analysis.•Ultrasound microstress led to weakened energy metabolism during post-fermentation.•Inhibited acidification related to UT-induced in energy metabolism and nutrient transport.•Ultrasound microstress reduced activities of H+-ATPase and lactate dehydrogenase.•UT stress evidenced by microstructure characterization of UT-stressed L. Bulgaricus.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>38839237</pmid><doi>10.1016/j.fm.2024.104563</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-4426-852X</orcidid></addata></record>
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source MEDLINE; Elsevier ScienceDirect Journals
subjects absorption
acidification
acyl carrier protein
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
energy
exposure duration
fatty acids
Fermentation
food microbiology
Gene Expression Profiling
glucose-6-phosphate isomerase
glycerol-3-phosphate dehydrogenase
glycolysis
Hydrogen-Ion Concentration
inoculum
lactate dehydrogenase
Lactic acid bacteria
Lactobacillus delbrueckii - genetics
Lactobacillus delbrueckii - metabolism
membrane permeability
membrane potential
Post-fermentation acidification
pyruvate oxidase
pyruvic acid
Sonication
Sono-biochemical control
Transcriptome
Transcriptomic analysis
transcriptomics
ultrasonic treatment
ultrasonics
yogurt
title Comparative physiological and transcriptomic analysis of sono-biochemical control over post-acidification of Lactobacillus delbrueckii subsp. bulgaricus
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