Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery
<p>Abstract</p> <p>Background</p> <p>Many <it>E. coli </it>genes show pH-dependent expression during logarithmic growth in acid (pH 5–6) or in base (pH 8–9). The effect of rapid pH change, however, has rarely been tested. Rapid acid treatment could distingui...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2008-02-01
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| Series: | BMC Microbiology |
| Online Access: | http://www.biomedcentral.com/1471-2180/8/37 |
| _version_ | 1818666675709411328 |
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| author | Jones Brian D Fitzgerald Devon M Wilks Jessica C Kannan Geetha BonDurant Sandra S Slonczewski Joan L |
| author_facet | Jones Brian D Fitzgerald Devon M Wilks Jessica C Kannan Geetha BonDurant Sandra S Slonczewski Joan L |
| author_sort | Jones Brian D |
| collection | DOAJ |
| description | <p>Abstract</p> <p>Background</p> <p>Many <it>E. coli </it>genes show pH-dependent expression during logarithmic growth in acid (pH 5–6) or in base (pH 8–9). The effect of rapid pH change, however, has rarely been tested. Rapid acid treatment could distinguish between genes responding to external pH, and genes responding to cytoplasmic acidification, which occurs transiently following rapid external acidification. It could reveal previously unknown acid-stress genes whose effects are transient, as well as show which acid-stress genes have a delayed response.</p> <p>Results</p> <p>Microarray hybridization was employed to observe the global gene expression of <it>E. coli </it>K-12 W3110 following rapid acidification of the external medium, from pH 7.6 to pH 5.5. Fluorimetric observation of pH-dependent tetR-YFP showed that rapid external acidification led to a half-unit drop in cytoplasmic pH (from pH 7.6 to pH 6.4) which began to recover within 20 s. Following acid treatment, 630 genes were up-regulated and 586 genes were down-regulated. Up-regulated genes included amino-acid decarboxylases (<it>cadA, adiY</it>, <it>gadA</it>), succinate dehydrogenase (<it>sdhABCD</it>), biofilm-associated genes (<it>bdm</it>, <it>gatAB</it>, and <it>ymgABC</it>), and the Gad, Fur and Rcs regulons. Genes with response patterns consistent with cytoplasmic acid stress were revealed by addition of benzoate, a membrane-permeant acid that permanently depresses cytoplasmic pH without affecting external pH. Several genes (<it>yagU</it>, <it>ygiN</it>, <it>yjeI</it>, and <it>yneI</it>) were up-regulated specifically by external acidification, while other genes (<it>fimB</it>, <it>ygaC</it>, <it>yhcN</it>, <it>yhjX</it>, <it>ymgABC</it>, <it>yodA</it>) presented a benzoate response consistent with cytoplasmic pH stress. Other genes (the <it>nuo </it>operon for NADH dehydrogenase I, and the HslUV protease) showed delayed up-regulation by acid, with expression rising by 10 min following the acid shift.</p> <p>Conclusion</p> <p>Transcriptomic profiling of <it>E. coli </it>K-12 distinguished three different classes of change in gene expression following rapid acid treatment: up-regulation with or without recovery, and delayed response to acid. For eight genes showing acid response and recovery (<it>fimB</it>, <it>ygaC</it>, <it>yhcN</it>, <it>yhjX</it>, <it>ymgABC</it>, <it>yodA</it>), responses to the permeant acid benzoate revealed expression patterns consistent with sensing of cytoplasmic pH. The delayed acid response of <it>nuo </it>genes shows that NADH dehydrogenase I is probably induced as a secondary result of acid-associated metabolism, not as a direct response to cytoplasmic acidification.</p> |
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| language | English |
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| publishDate | 2008-02-01 |
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| series | BMC Microbiology |
| spelling | doaj.art-f7c3f66763324487a5d0a662a797f93e2022-12-21T22:00:43ZengBMCBMC Microbiology1471-21802008-02-01813710.1186/1471-2180-8-37Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recoveryJones Brian DFitzgerald Devon MWilks Jessica CKannan GeethaBonDurant Sandra SSlonczewski Joan L<p>Abstract</p> <p>Background</p> <p>Many <it>E. coli </it>genes show pH-dependent expression during logarithmic growth in acid (pH 5–6) or in base (pH 8–9). The effect of rapid pH change, however, has rarely been tested. Rapid acid treatment could distinguish between genes responding to external pH, and genes responding to cytoplasmic acidification, which occurs transiently following rapid external acidification. It could reveal previously unknown acid-stress genes whose effects are transient, as well as show which acid-stress genes have a delayed response.</p> <p>Results</p> <p>Microarray hybridization was employed to observe the global gene expression of <it>E. coli </it>K-12 W3110 following rapid acidification of the external medium, from pH 7.6 to pH 5.5. Fluorimetric observation of pH-dependent tetR-YFP showed that rapid external acidification led to a half-unit drop in cytoplasmic pH (from pH 7.6 to pH 6.4) which began to recover within 20 s. Following acid treatment, 630 genes were up-regulated and 586 genes were down-regulated. Up-regulated genes included amino-acid decarboxylases (<it>cadA, adiY</it>, <it>gadA</it>), succinate dehydrogenase (<it>sdhABCD</it>), biofilm-associated genes (<it>bdm</it>, <it>gatAB</it>, and <it>ymgABC</it>), and the Gad, Fur and Rcs regulons. Genes with response patterns consistent with cytoplasmic acid stress were revealed by addition of benzoate, a membrane-permeant acid that permanently depresses cytoplasmic pH without affecting external pH. Several genes (<it>yagU</it>, <it>ygiN</it>, <it>yjeI</it>, and <it>yneI</it>) were up-regulated specifically by external acidification, while other genes (<it>fimB</it>, <it>ygaC</it>, <it>yhcN</it>, <it>yhjX</it>, <it>ymgABC</it>, <it>yodA</it>) presented a benzoate response consistent with cytoplasmic pH stress. Other genes (the <it>nuo </it>operon for NADH dehydrogenase I, and the HslUV protease) showed delayed up-regulation by acid, with expression rising by 10 min following the acid shift.</p> <p>Conclusion</p> <p>Transcriptomic profiling of <it>E. coli </it>K-12 distinguished three different classes of change in gene expression following rapid acid treatment: up-regulation with or without recovery, and delayed response to acid. For eight genes showing acid response and recovery (<it>fimB</it>, <it>ygaC</it>, <it>yhcN</it>, <it>yhjX</it>, <it>ymgABC</it>, <it>yodA</it>), responses to the permeant acid benzoate revealed expression patterns consistent with sensing of cytoplasmic pH. The delayed acid response of <it>nuo </it>genes shows that NADH dehydrogenase I is probably induced as a secondary result of acid-associated metabolism, not as a direct response to cytoplasmic acidification.</p>http://www.biomedcentral.com/1471-2180/8/37 |
| spellingShingle | Jones Brian D Fitzgerald Devon M Wilks Jessica C Kannan Geetha BonDurant Sandra S Slonczewski Joan L Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery BMC Microbiology |
| title | Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery |
| title_full | Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery |
| title_fullStr | Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery |
| title_full_unstemmed | Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery |
| title_short | Rapid acid treatment of <it>Escherichia coli</it>: transcriptomic response and recovery |
| title_sort | rapid acid treatment of it escherichia coli it transcriptomic response and recovery |
| url | http://www.biomedcentral.com/1471-2180/8/37 |
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