Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production
Acetic acid accumulation is a universal limiting factor to the vinegar manufacture because of the toxic effect of acetic acid on the acid producing strain, such as Acetobacter pasteurianu s. In this study, we aimed to investigate the genome-wide transcriptional response of A. pasteurianus Ab3 to hig...
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| Veröffentlicht in: | Applied microbiology and biotechnology 2020-12, Vol.104 (24), p.10585-10599 |
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| creator | Xia, Kai Han, Chengcheng Xu, Jun Liang, Xinle |
| description | Acetic acid accumulation is a universal limiting factor to the vinegar manufacture because of the toxic effect of acetic acid on the acid producing strain, such as
Acetobacter pasteurianu
s. In this study, we aimed to investigate the genome-wide transcriptional response of
A. pasteurianus
Ab3 to high acid stress during vinegar production. By comparing the transcriptional landscape of cells harvested from a long-term cultivation with high acidity (70 ± 3 g/L) to that of low acidity (10 ± 2 g/L), we demonstrated that 1005 genes were differentially expressed. By functional enrichment analysis, we found that the expression of genes related to the two-component systems (TCS) and toxin-antitoxin systems (TAS) was significantly regulated under high acid stress. Cells increased the genome stability to withstand the intracellular toxicity caused by the acetic acid accumulation by repressing the expression of transposases and integrases. Moreover, high acid stress induced the expression of genes involved in the pathways of peptidoglycan, ceramide, and phosphatidylcholine biosynthesis as well as the Tol-Pal and TonB-ExbB systems. In addition, we observed that cells increased and diversified the ATP production to resist high acid stress. Transcriptional upregulation in the pathways of pyrroloquinoline quinone (PQQ) synthesis and thiamine metabolism suggested that cells may increase the production of prosthetic groups to ensure the enzyme activity upon high acid stress. Collectively, the results of this study increase our current understanding of the acetic acid resistance (AAR) mechanisms in
A. pasteurianus
and provide opportunities for strain improvement and scaled-up vinegar production.
Key Points
•
TCS and TAS are responsive to the acid stress and constitute the regulating networks.
•
Adaptive expression changes of cell envelope elements help cell resist acid stress.
•
Cells promote genome stability and diversify ATP production to withstand acid stress. |
| doi_str_mv | 10.1007/s00253-020-10995-0 |
| format | Article |
| fullrecord | <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_journals_2471614506</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A642125901</galeid><sourcerecordid>A642125901</sourcerecordid><originalsourceid>FETCH-LOGICAL-c513t-516343fb639b7622da7f4da43604cff6a87e9bedfeb9fbc85cb11c23c937b33a3</originalsourceid><addsrcrecordid>eNp9kV1rFTEQhoMo9lj9A15IwKtebM33nr08FD8KBUHrdUiyk21qN1mTbNF_39RTLQdEcjEQnneGmQeh15ScUkL6d4UQJnlHGOkoGQbZkSdoQwVnHVFUPEUbQnvZ9XLYHqEXpVwTQtlWqefoiHMqlRBqg75fZhOLy2GpaQacoSwpFsDJ452DmqxxFTJeTKmw5mDiWvDOclwTvgrTFTYNCq6VMOJSW7zgsXFxwrchwmRaNKdxdTWk-BI98-amwKuHeoy-fXh_efapu_j88fxsd9E5SXntJFVccG8VH2yvGBtN78VoBFdEOO-V2fYwWBg92MFbt5XOUuoYdwPvLeeGH6O3-75t9I8VStXXac2xjdRM9LTdRhL1SE3mBnSIPtVs3ByK0zslGGVyILRRp_-g2hthDi5F8KH9HwRODgKNqfCzTmYtRZ9__XLIsj3rciolg9dLDrPJvzQl-l6x3ivWTbH-rViTFnrzsN1qZxj_Rv44bQDfA2W5FwH5cf3_tL0DA5-wiQ</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2471614506</pqid></control><display><type>article</type><title>Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production</title><source>MEDLINE</source><source>SpringerLink Journals - AutoHoldings</source><creator>Xia, Kai ; Han, Chengcheng ; Xu, Jun ; Liang, Xinle</creator><creatorcontrib>Xia, Kai ; Han, Chengcheng ; Xu, Jun ; Liang, Xinle</creatorcontrib><description>Acetic acid accumulation is a universal limiting factor to the vinegar manufacture because of the toxic effect of acetic acid on the acid producing strain, such as
Acetobacter pasteurianu
s. In this study, we aimed to investigate the genome-wide transcriptional response of
A. pasteurianus
Ab3 to high acid stress during vinegar production. By comparing the transcriptional landscape of cells harvested from a long-term cultivation with high acidity (70 ± 3 g/L) to that of low acidity (10 ± 2 g/L), we demonstrated that 1005 genes were differentially expressed. By functional enrichment analysis, we found that the expression of genes related to the two-component systems (TCS) and toxin-antitoxin systems (TAS) was significantly regulated under high acid stress. Cells increased the genome stability to withstand the intracellular toxicity caused by the acetic acid accumulation by repressing the expression of transposases and integrases. Moreover, high acid stress induced the expression of genes involved in the pathways of peptidoglycan, ceramide, and phosphatidylcholine biosynthesis as well as the Tol-Pal and TonB-ExbB systems. In addition, we observed that cells increased and diversified the ATP production to resist high acid stress. Transcriptional upregulation in the pathways of pyrroloquinoline quinone (PQQ) synthesis and thiamine metabolism suggested that cells may increase the production of prosthetic groups to ensure the enzyme activity upon high acid stress. Collectively, the results of this study increase our current understanding of the acetic acid resistance (AAR) mechanisms in
A. pasteurianus
and provide opportunities for strain improvement and scaled-up vinegar production.
Key Points
•
TCS and TAS are responsive to the acid stress and constitute the regulating networks.
•
Adaptive expression changes of cell envelope elements help cell resist acid stress.
•
Cells promote genome stability and diversify ATP production to withstand acid stress.</description><identifier>ISSN: 0175-7598</identifier><identifier>EISSN: 1432-0614</identifier><identifier>DOI: 10.1007/s00253-020-10995-0</identifier><identifier>PMID: 33156446</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Accumulation ; Acetic acid ; Acetic Acid - toxicity ; Acetobacter - genetics ; Acetobacter pasteurianus ; Acid resistance ; Acidity ; Acids ; Analysis ; Antitoxins ; ATP ; Biomedical and Life Sciences ; Biosynthesis ; Biotechnology ; Ceramide ; Cultivation ; Enzymatic activity ; Enzyme activity ; Fermentation ; Gene expression ; Genes ; Genetic aspects ; Genetic transcription ; Genomes ; Genomics ; Lecithin ; Life Sciences ; Microbial Genetics and Genomics ; Microbiology ; Peptidoglycans ; Phosphatidylcholine ; Physiological aspects ; Production processes ; Prostheses ; Prosthetic groups ; Proteobacteria ; Proteomics ; Pyrroloquinoline quinone ; Quinones ; Stability ; Strain ; Stress ; Thiamine ; Toxicity ; Toxins ; Transcription ; Transcriptome ; Transcriptomics ; Vinegar</subject><ispartof>Applied microbiology and biotechnology, 2020-12, Vol.104 (24), p.10585-10599</ispartof><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2020</rights><rights>COPYRIGHT 2020 Springer</rights><rights>Springer-Verlag GmbH Germany, part of Springer Nature 2020.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c513t-516343fb639b7622da7f4da43604cff6a87e9bedfeb9fbc85cb11c23c937b33a3</citedby><cites>FETCH-LOGICAL-c513t-516343fb639b7622da7f4da43604cff6a87e9bedfeb9fbc85cb11c23c937b33a3</cites><orcidid>0000-0003-3454-7496</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00253-020-10995-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00253-020-10995-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33156446$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xia, Kai</creatorcontrib><creatorcontrib>Han, Chengcheng</creatorcontrib><creatorcontrib>Xu, Jun</creatorcontrib><creatorcontrib>Liang, Xinle</creatorcontrib><title>Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production</title><title>Applied microbiology and biotechnology</title><addtitle>Appl Microbiol Biotechnol</addtitle><addtitle>Appl Microbiol Biotechnol</addtitle><description>Acetic acid accumulation is a universal limiting factor to the vinegar manufacture because of the toxic effect of acetic acid on the acid producing strain, such as
Acetobacter pasteurianu
s. In this study, we aimed to investigate the genome-wide transcriptional response of
A. pasteurianus
Ab3 to high acid stress during vinegar production. By comparing the transcriptional landscape of cells harvested from a long-term cultivation with high acidity (70 ± 3 g/L) to that of low acidity (10 ± 2 g/L), we demonstrated that 1005 genes were differentially expressed. By functional enrichment analysis, we found that the expression of genes related to the two-component systems (TCS) and toxin-antitoxin systems (TAS) was significantly regulated under high acid stress. Cells increased the genome stability to withstand the intracellular toxicity caused by the acetic acid accumulation by repressing the expression of transposases and integrases. Moreover, high acid stress induced the expression of genes involved in the pathways of peptidoglycan, ceramide, and phosphatidylcholine biosynthesis as well as the Tol-Pal and TonB-ExbB systems. In addition, we observed that cells increased and diversified the ATP production to resist high acid stress. Transcriptional upregulation in the pathways of pyrroloquinoline quinone (PQQ) synthesis and thiamine metabolism suggested that cells may increase the production of prosthetic groups to ensure the enzyme activity upon high acid stress. Collectively, the results of this study increase our current understanding of the acetic acid resistance (AAR) mechanisms in
A. pasteurianus
and provide opportunities for strain improvement and scaled-up vinegar production.
Key Points
•
TCS and TAS are responsive to the acid stress and constitute the regulating networks.
•
Adaptive expression changes of cell envelope elements help cell resist acid stress.
•
Cells promote genome stability and diversify ATP production to withstand acid stress.</description><subject>Accumulation</subject><subject>Acetic acid</subject><subject>Acetic Acid - toxicity</subject><subject>Acetobacter - genetics</subject><subject>Acetobacter pasteurianus</subject><subject>Acid resistance</subject><subject>Acidity</subject><subject>Acids</subject><subject>Analysis</subject><subject>Antitoxins</subject><subject>ATP</subject><subject>Biomedical and Life Sciences</subject><subject>Biosynthesis</subject><subject>Biotechnology</subject><subject>Ceramide</subject><subject>Cultivation</subject><subject>Enzymatic activity</subject><subject>Enzyme activity</subject><subject>Fermentation</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic transcription</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Lecithin</subject><subject>Life Sciences</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Peptidoglycans</subject><subject>Phosphatidylcholine</subject><subject>Physiological aspects</subject><subject>Production processes</subject><subject>Prostheses</subject><subject>Prosthetic groups</subject><subject>Proteobacteria</subject><subject>Proteomics</subject><subject>Pyrroloquinoline quinone</subject><subject>Quinones</subject><subject>Stability</subject><subject>Strain</subject><subject>Stress</subject><subject>Thiamine</subject><subject>Toxicity</subject><subject>Toxins</subject><subject>Transcription</subject><subject>Transcriptome</subject><subject>Transcriptomics</subject><subject>Vinegar</subject><issn>0175-7598</issn><issn>1432-0614</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kV1rFTEQhoMo9lj9A15IwKtebM33nr08FD8KBUHrdUiyk21qN1mTbNF_39RTLQdEcjEQnneGmQeh15ScUkL6d4UQJnlHGOkoGQbZkSdoQwVnHVFUPEUbQnvZ9XLYHqEXpVwTQtlWqefoiHMqlRBqg75fZhOLy2GpaQacoSwpFsDJ452DmqxxFTJeTKmw5mDiWvDOclwTvgrTFTYNCq6VMOJSW7zgsXFxwrchwmRaNKdxdTWk-BI98-amwKuHeoy-fXh_efapu_j88fxsd9E5SXntJFVccG8VH2yvGBtN78VoBFdEOO-V2fYwWBg92MFbt5XOUuoYdwPvLeeGH6O3-75t9I8VStXXac2xjdRM9LTdRhL1SE3mBnSIPtVs3ByK0zslGGVyILRRp_-g2hthDi5F8KH9HwRODgKNqfCzTmYtRZ9__XLIsj3rciolg9dLDrPJvzQl-l6x3ivWTbH-rViTFnrzsN1qZxj_Rv44bQDfA2W5FwH5cf3_tL0DA5-wiQ</recordid><startdate>20201201</startdate><enddate>20201201</enddate><creator>Xia, 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response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production</title><author>Xia, Kai ; Han, Chengcheng ; Xu, Jun ; Liang, Xinle</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-516343fb639b7622da7f4da43604cff6a87e9bedfeb9fbc85cb11c23c937b33a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Accumulation</topic><topic>Acetic acid</topic><topic>Acetic Acid - toxicity</topic><topic>Acetobacter - genetics</topic><topic>Acetobacter pasteurianus</topic><topic>Acid resistance</topic><topic>Acidity</topic><topic>Acids</topic><topic>Analysis</topic><topic>Antitoxins</topic><topic>ATP</topic><topic>Biomedical and Life Sciences</topic><topic>Biosynthesis</topic><topic>Biotechnology</topic><topic>Ceramide</topic><topic>Cultivation</topic><topic>Enzymatic activity</topic><topic>Enzyme activity</topic><topic>Fermentation</topic><topic>Gene 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Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Business</collection><collection>ProQuest One Business (Alumni)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><jtitle>Applied microbiology and biotechnology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xia, Kai</au><au>Han, Chengcheng</au><au>Xu, Jun</au><au>Liang, Xinle</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production</atitle><jtitle>Applied microbiology and biotechnology</jtitle><stitle>Appl Microbiol Biotechnol</stitle><addtitle>Appl Microbiol Biotechnol</addtitle><date>2020-12-01</date><risdate>2020</risdate><volume>104</volume><issue>24</issue><spage>10585</spage><epage>10599</epage><pages>10585-10599</pages><issn>0175-7598</issn><eissn>1432-0614</eissn><abstract>Acetic acid accumulation is a universal limiting factor to the vinegar manufacture because of the toxic effect of acetic acid on the acid producing strain, such as
Acetobacter pasteurianu
s. In this study, we aimed to investigate the genome-wide transcriptional response of
A. pasteurianus
Ab3 to high acid stress during vinegar production. By comparing the transcriptional landscape of cells harvested from a long-term cultivation with high acidity (70 ± 3 g/L) to that of low acidity (10 ± 2 g/L), we demonstrated that 1005 genes were differentially expressed. By functional enrichment analysis, we found that the expression of genes related to the two-component systems (TCS) and toxin-antitoxin systems (TAS) was significantly regulated under high acid stress. Cells increased the genome stability to withstand the intracellular toxicity caused by the acetic acid accumulation by repressing the expression of transposases and integrases. Moreover, high acid stress induced the expression of genes involved in the pathways of peptidoglycan, ceramide, and phosphatidylcholine biosynthesis as well as the Tol-Pal and TonB-ExbB systems. In addition, we observed that cells increased and diversified the ATP production to resist high acid stress. Transcriptional upregulation in the pathways of pyrroloquinoline quinone (PQQ) synthesis and thiamine metabolism suggested that cells may increase the production of prosthetic groups to ensure the enzyme activity upon high acid stress. Collectively, the results of this study increase our current understanding of the acetic acid resistance (AAR) mechanisms in
A. pasteurianus
and provide opportunities for strain improvement and scaled-up vinegar production.
Key Points
•
TCS and TAS are responsive to the acid stress and constitute the regulating networks.
•
Adaptive expression changes of cell envelope elements help cell resist acid stress.
•
Cells promote genome stability and diversify ATP production to withstand acid stress.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>33156446</pmid><doi>10.1007/s00253-020-10995-0</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-3454-7496</orcidid></addata></record> |
| fulltext | fulltext |
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| ispartof | Applied microbiology and biotechnology, 2020-12, Vol.104 (24), p.10585-10599 |
| issn | 0175-7598 1432-0614 |
| language | eng |
| recordid | cdi_proquest_journals_2471614506 |
| source | MEDLINE; SpringerLink Journals - AutoHoldings |
| subjects | Accumulation Acetic acid Acetic Acid - toxicity Acetobacter - genetics Acetobacter pasteurianus Acid resistance Acidity Acids Analysis Antitoxins ATP Biomedical and Life Sciences Biosynthesis Biotechnology Ceramide Cultivation Enzymatic activity Enzyme activity Fermentation Gene expression Genes Genetic aspects Genetic transcription Genomes Genomics Lecithin Life Sciences Microbial Genetics and Genomics Microbiology Peptidoglycans Phosphatidylcholine Physiological aspects Production processes Prostheses Prosthetic groups Proteobacteria Proteomics Pyrroloquinoline quinone Quinones Stability Strain Stress Thiamine Toxicity Toxins Transcription Transcriptome Transcriptomics Vinegar |
| title | Transcriptome response of Acetobacter pasteurianus Ab3 to high acetic acid stress during vinegar production |
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