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Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor
Cells reprogram their transcriptome in response to stress, such as heat shock. In free-living bacteria, the transcriptomic reprogramming is mediated by increased DNA-binding activity of heat shock sigma factors and activation of genes normally repressed by heat-induced transcription factors. In this...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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Frontiers Media S.A.
2022
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8762339/ https://www.ncbi.nlm.nih.gov/pubmed/35046926 http://dx.doi.org/10.3389/fmicb.2021.812448 |
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author | Huang, Yehong Wurihan, Wurihan Lu, Bin Zou, Yi Wang, Yuxuan Weldon, Korri Fondell, Joseph D. Lai, Zhao Wu, Xiang Fan, Huizhou |
author_facet | Huang, Yehong Wurihan, Wurihan Lu, Bin Zou, Yi Wang, Yuxuan Weldon, Korri Fondell, Joseph D. Lai, Zhao Wu, Xiang Fan, Huizhou |
author_sort | Huang, Yehong |
collection | PubMed |
description | Cells reprogram their transcriptome in response to stress, such as heat shock. In free-living bacteria, the transcriptomic reprogramming is mediated by increased DNA-binding activity of heat shock sigma factors and activation of genes normally repressed by heat-induced transcription factors. In this study, we performed transcriptomic analyses to investigate heat shock response in the obligate intracellular bacterium Chlamydia trachomatis, whose genome encodes only three sigma factors and a single heat-induced transcription factor. Nearly one-third of C. trachomatis genes showed statistically significant (≥1.5-fold) expression changes 30 min after shifting from 37 to 45°C. Notably, chromosomal genes encoding chaperones, energy metabolism enzymes, type III secretion proteins, as well as most plasmid-encoded genes, were differentially upregulated. In contrast, genes with functions in protein synthesis were disproportionately downregulated. These findings suggest that facilitating protein folding, increasing energy production, manipulating host activities, upregulating plasmid-encoded gene expression, and decreasing general protein synthesis helps facilitate C. trachomatis survival under stress. In addition to relieving negative regulation by the heat-inducible transcriptional repressor HrcA, heat shock upregulated the chlamydial primary sigma factor σ(66) and an alternative sigma factor σ(28). Interestingly, we show for the first time that heat shock downregulates the other alternative sigma factor σ(54) in a bacterium. Downregulation of σ(54) was accompanied by increased expression of the σ(54) RNA polymerase activator AtoC, thus suggesting a unique regulatory mechanism for reestablishing normal expression of select σ(54) target genes. Taken together, our findings reveal that C. trachomatis utilizes multiple novel survival strategies to cope with environmental stress and even to replicate. Future strategies that can specifically target and disrupt Chlamydia’s heat shock response will likely be of therapeutic value. |
format | Online Article Text |
id | pubmed-8762339 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-87623392022-01-18 Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor Huang, Yehong Wurihan, Wurihan Lu, Bin Zou, Yi Wang, Yuxuan Weldon, Korri Fondell, Joseph D. Lai, Zhao Wu, Xiang Fan, Huizhou Front Microbiol Microbiology Cells reprogram their transcriptome in response to stress, such as heat shock. In free-living bacteria, the transcriptomic reprogramming is mediated by increased DNA-binding activity of heat shock sigma factors and activation of genes normally repressed by heat-induced transcription factors. In this study, we performed transcriptomic analyses to investigate heat shock response in the obligate intracellular bacterium Chlamydia trachomatis, whose genome encodes only three sigma factors and a single heat-induced transcription factor. Nearly one-third of C. trachomatis genes showed statistically significant (≥1.5-fold) expression changes 30 min after shifting from 37 to 45°C. Notably, chromosomal genes encoding chaperones, energy metabolism enzymes, type III secretion proteins, as well as most plasmid-encoded genes, were differentially upregulated. In contrast, genes with functions in protein synthesis were disproportionately downregulated. These findings suggest that facilitating protein folding, increasing energy production, manipulating host activities, upregulating plasmid-encoded gene expression, and decreasing general protein synthesis helps facilitate C. trachomatis survival under stress. In addition to relieving negative regulation by the heat-inducible transcriptional repressor HrcA, heat shock upregulated the chlamydial primary sigma factor σ(66) and an alternative sigma factor σ(28). Interestingly, we show for the first time that heat shock downregulates the other alternative sigma factor σ(54) in a bacterium. Downregulation of σ(54) was accompanied by increased expression of the σ(54) RNA polymerase activator AtoC, thus suggesting a unique regulatory mechanism for reestablishing normal expression of select σ(54) target genes. Taken together, our findings reveal that C. trachomatis utilizes multiple novel survival strategies to cope with environmental stress and even to replicate. Future strategies that can specifically target and disrupt Chlamydia’s heat shock response will likely be of therapeutic value. Frontiers Media S.A. 2022-01-03 /pmc/articles/PMC8762339/ /pubmed/35046926 http://dx.doi.org/10.3389/fmicb.2021.812448 Text en Copyright © 2022 Huang, Wurihan, Lu, Zou, Wang, Weldon, Fondell, Lai, Wu and Fan. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Huang, Yehong Wurihan, Wurihan Lu, Bin Zou, Yi Wang, Yuxuan Weldon, Korri Fondell, Joseph D. Lai, Zhao Wu, Xiang Fan, Huizhou Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title | Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title_full | Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title_fullStr | Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title_full_unstemmed | Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title_short | Robust Heat Shock Response in Chlamydia Lacking a Typical Heat Shock Sigma Factor |
title_sort | robust heat shock response in chlamydia lacking a typical heat shock sigma factor |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8762339/ https://www.ncbi.nlm.nih.gov/pubmed/35046926 http://dx.doi.org/10.3389/fmicb.2021.812448 |
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