Effects of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis
Lactiplantibacillus plantarum is frequently exposed to salt stress during industrial applications. Catabolite control protein (CcpA) controls the transcription of many genes, but its role in the response to salt stress remains unclear. In this study, we used transcriptome analyses to investigate dif...
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creator | Chen, Chen Huang, Ke Li, Xiaohong Tian, Huaixiang Yu, Haiyan Huang, Juan Yuan, Haibin Zhao, Shanshan Shao, Li |
description | Lactiplantibacillus plantarum
is frequently exposed to salt stress during industrial applications. Catabolite control protein (CcpA) controls the transcription of many genes, but its role in the response to salt stress remains unclear. In this study, we used transcriptome analyses to investigate differences in the logarithmic growth phases of
Lactiplantibacillus plantarum
ST-III and its
ccpA
-knockout mutant when grown with or without salt and glycine betaine (GB). The deletion of
ccpA
significantly affected bacterial growth under different conditions. Among the comparisons, the highest proportion of differentially expressed genes (64%) was observed in the comparison between the wild-type and
ccpA
mutant grown with NaCl, whereas the lowest proportion (6%) was observed in the comparison between the
ccpA
mutant strain cultures grown with NaCl alone or with GB together. Transcriptomic analyses showed that CcpA could regulate GB uptake, activate iron uptake, produce acetyl-CoA, and affect fatty acid composition to maintain membrane lipid homeostasis in the adaptation of high-salinity conditions. Conclusively, these results demonstrate the importance of CcpA as a master regulator of these processes in response to salt stress, and provide new insights into the complex regulatory network of lactic acid bacteria.
Key points
• The absence of CcpA significantly affected growth of L. plantarum and its response to salt stress.
• CcpA regulates compatible solutes absorption and ions transport to resist salt stress.
• CcpA alters fatty acids composition to maintain membrane lipid homeostasis towards salt stress.
Graphical abstract |
doi_str_mv | 10.1007/s00253-021-11276-0 |
format | Article |
fullrecord | <record><control><sourceid>gale_webof</sourceid><recordid>TN_cdi_webofscience_primary_000640154800001</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A661043430</galeid><sourcerecordid>A661043430</sourcerecordid><originalsourceid>FETCH-LOGICAL-c513t-38e4ca53021e5d8125484df3df96d7d012036ae8d2aad4eda97ea9691b4175973</originalsourceid><addsrcrecordid>eNqNkltrVDEQxw-i2G31C_ggAV8scuokOdfHZalaWBC8PIfZnDlLyrmZyandb2-2W1tWRCQhN37_Yf6TSZJXEi4kQPmeAVSuU1AylVKVRQpPkoXMtEqhkNnTZAGyzNMyr6uT5JT5GkCqqiieJydaV7kClS2S28u2JRtYjK1Y2WkpcItu4CAYu7gET8zCDWKNNripwyG4DVrXdTOLuyv6uRfIcXJEqRGbnbBjP6HH4G5IBI8DW--m4MYBO4Fx2bHjF8mzFjuml_f7WfL9w-W31ad0_fnj1Wq5Tm0udUh1RZnFXEeTlDeVVHlWZU2rm7YumrKJjkAXSFWjEJuMGqxLwrqo5SaL5utSnyVvD3EnP_6YiYPpHVvqYu40zmxUHkuntaqriL75A70eZx_z3VNK5QB5VT9SW-zIuKEdo0W7D2qWRSEh05mGSF38hYqjod7ZcaDWxfcjwfmRIDKBbsMWZ2Zz9fXLMasOrPUjs6fWTN716HdGgtm3hjm0holVM3etYfai1_fu5k1PzYPkdy9E4N0B-EmbsWXraLD0gAFAkYGM5Y8nkJGu_p9euYD7_1-N8xCiVB-kHPFhS_6xzv_I_xctXOMI</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2522500589</pqid></control><display><type>article</type><title>Effects of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis</title><source>SpringerNature Journals</source><creator>Chen, Chen ; Huang, Ke ; Li, Xiaohong ; Tian, Huaixiang ; Yu, Haiyan ; Huang, Juan ; Yuan, Haibin ; Zhao, Shanshan ; Shao, Li</creator><creatorcontrib>Chen, Chen ; Huang, Ke ; Li, Xiaohong ; Tian, Huaixiang ; Yu, Haiyan ; Huang, Juan ; Yuan, Haibin ; Zhao, Shanshan ; Shao, Li</creatorcontrib><description>Lactiplantibacillus plantarum
is frequently exposed to salt stress during industrial applications. Catabolite control protein (CcpA) controls the transcription of many genes, but its role in the response to salt stress remains unclear. In this study, we used transcriptome analyses to investigate differences in the logarithmic growth phases of
Lactiplantibacillus plantarum
ST-III and its
ccpA
-knockout mutant when grown with or without salt and glycine betaine (GB). The deletion of
ccpA
significantly affected bacterial growth under different conditions. Among the comparisons, the highest proportion of differentially expressed genes (64%) was observed in the comparison between the wild-type and
ccpA
mutant grown with NaCl, whereas the lowest proportion (6%) was observed in the comparison between the
ccpA
mutant strain cultures grown with NaCl alone or with GB together. Transcriptomic analyses showed that CcpA could regulate GB uptake, activate iron uptake, produce acetyl-CoA, and affect fatty acid composition to maintain membrane lipid homeostasis in the adaptation of high-salinity conditions. Conclusively, these results demonstrate the importance of CcpA as a master regulator of these processes in response to salt stress, and provide new insights into the complex regulatory network of lactic acid bacteria.
Key points
• The absence of CcpA significantly affected growth of L. plantarum and its response to salt stress.
• CcpA regulates compatible solutes absorption and ions transport to resist salt stress.
• CcpA alters fatty acids composition to maintain membrane lipid homeostasis towards salt stress.
Graphical abstract</description><identifier>ISSN: 0175-7598</identifier><identifier>EISSN: 1432-0614</identifier><identifier>DOI: 10.1007/s00253-021-11276-0</identifier><identifier>PMID: 33852024</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Abiotic stress ; Bacteria ; Biomedical and Life Sciences ; Biotechnology ; Biotechnology & Applied Microbiology ; Composition ; DNA binding proteins ; Fatty acid composition ; Fatty acids ; Gene expression ; Genes ; Genetic aspects ; Genomics ; Glycine ; Glycine betaine ; Homeostasis ; Industrial applications ; Lactic acid ; Lactic acid bacteria ; Lactobacillus plantarum ; Life Sciences ; Life Sciences & Biomedicine ; Lipids ; Membranes ; Microbial Genetics and Genomics ; Microbiology ; Mutants ; Osmosis ; Physiological aspects ; Proteomics ; Salinity tolerance ; Salts ; Science & Technology ; Sodium chloride ; Solutes ; Stress (Physiology) ; Transcription ; Transcriptomes ; Transcriptomics ; Yeast</subject><ispartof>Applied microbiology and biotechnology, 2021-05, Vol.105 (9), p.3691-3704</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021</rights><rights>COPYRIGHT 2021 Springer</rights><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>5</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000640154800001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c513t-38e4ca53021e5d8125484df3df96d7d012036ae8d2aad4eda97ea9691b4175973</citedby><cites>FETCH-LOGICAL-c513t-38e4ca53021e5d8125484df3df96d7d012036ae8d2aad4eda97ea9691b4175973</cites><orcidid>0000-0001-8255-4362</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/s00253-021-11276-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00253-021-11276-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,781,785,27928,27929,41492,42561,51323</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33852024$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Chen</creatorcontrib><creatorcontrib>Huang, Ke</creatorcontrib><creatorcontrib>Li, Xiaohong</creatorcontrib><creatorcontrib>Tian, Huaixiang</creatorcontrib><creatorcontrib>Yu, Haiyan</creatorcontrib><creatorcontrib>Huang, Juan</creatorcontrib><creatorcontrib>Yuan, Haibin</creatorcontrib><creatorcontrib>Zhao, Shanshan</creatorcontrib><creatorcontrib>Shao, Li</creatorcontrib><title>Effects of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis</title><title>Applied microbiology and biotechnology</title><addtitle>Appl Microbiol Biotechnol</addtitle><addtitle>APPL MICROBIOL BIOT</addtitle><addtitle>Appl Microbiol Biotechnol</addtitle><description>Lactiplantibacillus plantarum
is frequently exposed to salt stress during industrial applications. Catabolite control protein (CcpA) controls the transcription of many genes, but its role in the response to salt stress remains unclear. In this study, we used transcriptome analyses to investigate differences in the logarithmic growth phases of
Lactiplantibacillus plantarum
ST-III and its
ccpA
-knockout mutant when grown with or without salt and glycine betaine (GB). The deletion of
ccpA
significantly affected bacterial growth under different conditions. Among the comparisons, the highest proportion of differentially expressed genes (64%) was observed in the comparison between the wild-type and
ccpA
mutant grown with NaCl, whereas the lowest proportion (6%) was observed in the comparison between the
ccpA
mutant strain cultures grown with NaCl alone or with GB together. Transcriptomic analyses showed that CcpA could regulate GB uptake, activate iron uptake, produce acetyl-CoA, and affect fatty acid composition to maintain membrane lipid homeostasis in the adaptation of high-salinity conditions. Conclusively, these results demonstrate the importance of CcpA as a master regulator of these processes in response to salt stress, and provide new insights into the complex regulatory network of lactic acid bacteria.
Key points
• The absence of CcpA significantly affected growth of L. plantarum and its response to salt stress.
• CcpA regulates compatible solutes absorption and ions transport to resist salt stress.
• CcpA alters fatty acids composition to maintain membrane lipid homeostasis towards salt stress.
Graphical abstract</description><subject>Abiotic stress</subject><subject>Bacteria</subject><subject>Biomedical and Life Sciences</subject><subject>Biotechnology</subject><subject>Biotechnology & Applied Microbiology</subject><subject>Composition</subject><subject>DNA binding proteins</subject><subject>Fatty acid composition</subject><subject>Fatty acids</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomics</subject><subject>Glycine</subject><subject>Glycine betaine</subject><subject>Homeostasis</subject><subject>Industrial applications</subject><subject>Lactic acid</subject><subject>Lactic acid bacteria</subject><subject>Lactobacillus plantarum</subject><subject>Life Sciences</subject><subject>Life Sciences & Biomedicine</subject><subject>Lipids</subject><subject>Membranes</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Mutants</subject><subject>Osmosis</subject><subject>Physiological aspects</subject><subject>Proteomics</subject><subject>Salinity tolerance</subject><subject>Salts</subject><subject>Science & Technology</subject><subject>Sodium chloride</subject><subject>Solutes</subject><subject>Stress (Physiology)</subject><subject>Transcription</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><subject>Yeast</subject><issn>0175-7598</issn><issn>1432-0614</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqNkltrVDEQxw-i2G31C_ggAV8scuokOdfHZalaWBC8PIfZnDlLyrmZyandb2-2W1tWRCQhN37_Yf6TSZJXEi4kQPmeAVSuU1AylVKVRQpPkoXMtEqhkNnTZAGyzNMyr6uT5JT5GkCqqiieJydaV7kClS2S28u2JRtYjK1Y2WkpcItu4CAYu7gET8zCDWKNNripwyG4DVrXdTOLuyv6uRfIcXJEqRGbnbBjP6HH4G5IBI8DW--m4MYBO4Fx2bHjF8mzFjuml_f7WfL9w-W31ad0_fnj1Wq5Tm0udUh1RZnFXEeTlDeVVHlWZU2rm7YumrKJjkAXSFWjEJuMGqxLwrqo5SaL5utSnyVvD3EnP_6YiYPpHVvqYu40zmxUHkuntaqriL75A70eZx_z3VNK5QB5VT9SW-zIuKEdo0W7D2qWRSEh05mGSF38hYqjod7ZcaDWxfcjwfmRIDKBbsMWZ2Zz9fXLMasOrPUjs6fWTN716HdGgtm3hjm0holVM3etYfai1_fu5k1PzYPkdy9E4N0B-EmbsWXraLD0gAFAkYGM5Y8nkJGu_p9euYD7_1-N8xCiVB-kHPFhS_6xzv_I_xctXOMI</recordid><startdate>20210501</startdate><enddate>20210501</enddate><creator>Chen, 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of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis</title><author>Chen, Chen ; Huang, Ke ; Li, Xiaohong ; Tian, Huaixiang ; Yu, Haiyan ; Huang, Juan ; Yuan, Haibin ; Zhao, Shanshan ; Shao, Li</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-38e4ca53021e5d8125484df3df96d7d012036ae8d2aad4eda97ea9691b4175973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abiotic stress</topic><topic>Bacteria</topic><topic>Biomedical and Life Sciences</topic><topic>Biotechnology</topic><topic>Biotechnology & Applied Microbiology</topic><topic>Composition</topic><topic>DNA binding proteins</topic><topic>Fatty acid composition</topic><topic>Fatty acids</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomics</topic><topic>Glycine</topic><topic>Glycine betaine</topic><topic>Homeostasis</topic><topic>Industrial applications</topic><topic>Lactic acid</topic><topic>Lactic acid bacteria</topic><topic>Lactobacillus plantarum</topic><topic>Life Sciences</topic><topic>Life Sciences & Biomedicine</topic><topic>Lipids</topic><topic>Membranes</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Mutants</topic><topic>Osmosis</topic><topic>Physiological aspects</topic><topic>Proteomics</topic><topic>Salinity tolerance</topic><topic>Salts</topic><topic>Science & Technology</topic><topic>Sodium chloride</topic><topic>Solutes</topic><topic>Stress (Physiology)</topic><topic>Transcription</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Chen</creatorcontrib><creatorcontrib>Huang, Ke</creatorcontrib><creatorcontrib>Li, Xiaohong</creatorcontrib><creatorcontrib>Tian, Huaixiang</creatorcontrib><creatorcontrib>Yu, Haiyan</creatorcontrib><creatorcontrib>Huang, Juan</creatorcontrib><creatorcontrib>Yuan, Haibin</creatorcontrib><creatorcontrib>Zhao, Shanshan</creatorcontrib><creatorcontrib>Shao, Li</creatorcontrib><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>Web of Science - Science Citation Index Expanded - 2021</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Access via ABI/INFORM (ProQuest)</collection><collection>ABI/INFORM Global (PDF only)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 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Ke</au><au>Li, Xiaohong</au><au>Tian, Huaixiang</au><au>Yu, Haiyan</au><au>Huang, Juan</au><au>Yuan, Haibin</au><au>Zhao, Shanshan</au><au>Shao, Li</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Effects of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis</atitle><jtitle>Applied microbiology and biotechnology</jtitle><stitle>Appl Microbiol Biotechnol</stitle><stitle>APPL MICROBIOL BIOT</stitle><addtitle>Appl Microbiol Biotechnol</addtitle><date>2021-05-01</date><risdate>2021</risdate><volume>105</volume><issue>9</issue><spage>3691</spage><epage>3704</epage><pages>3691-3704</pages><issn>0175-7598</issn><eissn>1432-0614</eissn><abstract>Lactiplantibacillus plantarum
is frequently exposed to salt stress during industrial applications. Catabolite control protein (CcpA) controls the transcription of many genes, but its role in the response to salt stress remains unclear. In this study, we used transcriptome analyses to investigate differences in the logarithmic growth phases of
Lactiplantibacillus plantarum
ST-III and its
ccpA
-knockout mutant when grown with or without salt and glycine betaine (GB). The deletion of
ccpA
significantly affected bacterial growth under different conditions. Among the comparisons, the highest proportion of differentially expressed genes (64%) was observed in the comparison between the wild-type and
ccpA
mutant grown with NaCl, whereas the lowest proportion (6%) was observed in the comparison between the
ccpA
mutant strain cultures grown with NaCl alone or with GB together. Transcriptomic analyses showed that CcpA could regulate GB uptake, activate iron uptake, produce acetyl-CoA, and affect fatty acid composition to maintain membrane lipid homeostasis in the adaptation of high-salinity conditions. Conclusively, these results demonstrate the importance of CcpA as a master regulator of these processes in response to salt stress, and provide new insights into the complex regulatory network of lactic acid bacteria.
Key points
• The absence of CcpA significantly affected growth of L. plantarum and its response to salt stress.
• CcpA regulates compatible solutes absorption and ions transport to resist salt stress.
• CcpA alters fatty acids composition to maintain membrane lipid homeostasis towards salt stress.
Graphical abstract</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>33852024</pmid><doi>10.1007/s00253-021-11276-0</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8255-4362</orcidid></addata></record> |
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subjects | Abiotic stress Bacteria Biomedical and Life Sciences Biotechnology Biotechnology & Applied Microbiology Composition DNA binding proteins Fatty acid composition Fatty acids Gene expression Genes Genetic aspects Genomics Glycine Glycine betaine Homeostasis Industrial applications Lactic acid Lactic acid bacteria Lactobacillus plantarum Life Sciences Life Sciences & Biomedicine Lipids Membranes Microbial Genetics and Genomics Microbiology Mutants Osmosis Physiological aspects Proteomics Salinity tolerance Salts Science & Technology Sodium chloride Solutes Stress (Physiology) Transcription Transcriptomes Transcriptomics Yeast |
title | Effects of CcpA against salt stress in Lactiplantibacillus plantarum as assessed by comparative transcriptional analysis |
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