Tracking the Elusive Function of Bacillus subtilis Hfq
RNA-binding protein Hfq is a key component of the adaptive responses of many proteobacterial species including Escherichia coli, Salmonella enterica and Vibrio cholera. In these organisms, the importance of Hfq largely stems from its participation to regulatory mechanisms involving small non-coding...
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| creator | Rochat, Tatiana Delumeau, Olivier Figueroa-Bossi, Nara Noirot, Philippe Bossi, Lionello Dervyn, Etienne Bouloc, Philippe |
| description | RNA-binding protein Hfq is a key component of the adaptive responses of many proteobacterial species including Escherichia coli, Salmonella enterica and Vibrio cholera. In these organisms, the importance of Hfq largely stems from its participation to regulatory mechanisms involving small non-coding RNAs. In contrast, the function of Hfq in Gram-positive bacteria has remained elusive and somewhat controversial. In the present study, we have further addressed this point by comparing growth phenotypes and transcription profiles between wild-type and an hfq deletion mutant of the model Gram-positive bacterium, Bacillus subtilis. The absence of Hfq had no significant consequences on growth rates under nearly two thousand metabolic conditions and chemical treatments. The only phenotypic difference was a survival defect of B. subtilis hfq mutant in rich medium in stationary phase. Transcriptomic analysis correlated this phenotype with a change in the levels of nearly one hundred transcripts. Albeit a significant fraction of these RNAs (36%) encoded sporulation-related functions, analyses in a strain unable to sporulate ruled out sporulation per se as the basis of the hfq mutant's stationary phase fitness defect. When expressed in Salmonella, B. subtilis hfq complemented the sharp loss of viability of a degP hfq double mutant, attenuating the chronic σE-activated phenotype of this strain. However, B. subtilis hfq did not complement other regulatory deficiencies resulting from loss of Hfq-dependent small RNA activity in Salmonella indicating a limited functional overlap between Salmonella and B. subtilis Hfqs. Overall, this study confirmed that, despite structural similarities with other Hfq proteins, B. subtilis Hfq does not play a central role in post-transcriptional regulation but might have a more specialized function connected with stationary phase physiology. This would account for the high degree of conservation of Hfq proteins in all 17 B. subtilis strains whose genomes have been sequenced. |
| doi_str_mv | 10.1371/journal.pone.0124977 |
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In these organisms, the importance of Hfq largely stems from its participation to regulatory mechanisms involving small non-coding RNAs. In contrast, the function of Hfq in Gram-positive bacteria has remained elusive and somewhat controversial. In the present study, we have further addressed this point by comparing growth phenotypes and transcription profiles between wild-type and an hfq deletion mutant of the model Gram-positive bacterium, Bacillus subtilis. The absence of Hfq had no significant consequences on growth rates under nearly two thousand metabolic conditions and chemical treatments. The only phenotypic difference was a survival defect of B. subtilis hfq mutant in rich medium in stationary phase. Transcriptomic analysis correlated this phenotype with a change in the levels of nearly one hundred transcripts. Albeit a significant fraction of these RNAs (36%) encoded sporulation-related functions, analyses in a strain unable to sporulate ruled out sporulation per se as the basis of the hfq mutant's stationary phase fitness defect. When expressed in Salmonella, B. subtilis hfq complemented the sharp loss of viability of a degP hfq double mutant, attenuating the chronic σE-activated phenotype of this strain. However, B. subtilis hfq did not complement other regulatory deficiencies resulting from loss of Hfq-dependent small RNA activity in Salmonella indicating a limited functional overlap between Salmonella and B. subtilis Hfqs. Overall, this study confirmed that, despite structural similarities with other Hfq proteins, B. subtilis Hfq does not play a central role in post-transcriptional regulation but might have a more specialized function connected with stationary phase physiology. This would account for the high degree of conservation of Hfq proteins in all 17 B. subtilis strains whose genomes have been sequenced.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0124977</identifier><identifier>PMID: 25915524</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Bacillus subtilis ; Bacillus subtilis - genetics ; Bacillus subtilis - metabolism ; Bacteria ; Biology ; Chemical treatment ; Cholera ; Conservation ; Correlation analysis ; Deletion mutant ; E coli ; Escherichia coli ; Fitness ; Gene expression ; Gene regulation ; Genetic engineering ; Genomes ; Genomics ; Gram-positive bacteria ; Growth rate ; Homeostasis ; Host Factor 1 Protein - genetics ; Host Factor 1 Protein - metabolism ; Laboratories ; Life Sciences ; Organic chemistry ; Phenotype ; Phenotypes ; Physiological aspects ; Physiology ; Post-transcription ; Protein binding ; Proteins ; Regulatory mechanisms (biology) ; Ribonucleic acid ; RNA ; RNA-binding protein ; Salmonella ; Sporulation ; Staphylococcus aureus ; Stationary phase ; Strain analysis ; Studies ; Transcriptome ; Viability</subject><ispartof>PloS one, 2015-04, Vol.10 (4), p.e0124977-e0124977</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Rochat et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Attribution</rights><rights>2015 Rochat et al 2015 Rochat et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-32c2c5a6ed6820499bed062622eeb5d778e60c4dd70fcf0665473b0054ce9bc23</citedby><cites>FETCH-LOGICAL-c726t-32c2c5a6ed6820499bed062622eeb5d778e60c4dd70fcf0665473b0054ce9bc23</cites><orcidid>0000-0003-3446-6987 ; 0000-0002-4533-1220 ; 0000-0003-4601-3387 ; 0000-0002-7732-9491</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4410918/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4410918/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25915524$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01204479$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Rochat, Tatiana</creatorcontrib><creatorcontrib>Delumeau, Olivier</creatorcontrib><creatorcontrib>Figueroa-Bossi, Nara</creatorcontrib><creatorcontrib>Noirot, Philippe</creatorcontrib><creatorcontrib>Bossi, Lionello</creatorcontrib><creatorcontrib>Dervyn, Etienne</creatorcontrib><creatorcontrib>Bouloc, Philippe</creatorcontrib><title>Tracking the Elusive Function of Bacillus subtilis Hfq</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>RNA-binding protein Hfq is a key component of the adaptive responses of many proteobacterial species including Escherichia coli, Salmonella enterica and Vibrio cholera. In these organisms, the importance of Hfq largely stems from its participation to regulatory mechanisms involving small non-coding RNAs. In contrast, the function of Hfq in Gram-positive bacteria has remained elusive and somewhat controversial. In the present study, we have further addressed this point by comparing growth phenotypes and transcription profiles between wild-type and an hfq deletion mutant of the model Gram-positive bacterium, Bacillus subtilis. The absence of Hfq had no significant consequences on growth rates under nearly two thousand metabolic conditions and chemical treatments. The only phenotypic difference was a survival defect of B. subtilis hfq mutant in rich medium in stationary phase. Transcriptomic analysis correlated this phenotype with a change in the levels of nearly one hundred transcripts. Albeit a significant fraction of these RNAs (36%) encoded sporulation-related functions, analyses in a strain unable to sporulate ruled out sporulation per se as the basis of the hfq mutant's stationary phase fitness defect. When expressed in Salmonella, B. subtilis hfq complemented the sharp loss of viability of a degP hfq double mutant, attenuating the chronic σE-activated phenotype of this strain. However, B. subtilis hfq did not complement other regulatory deficiencies resulting from loss of Hfq-dependent small RNA activity in Salmonella indicating a limited functional overlap between Salmonella and B. subtilis Hfqs. Overall, this study confirmed that, despite structural similarities with other Hfq proteins, B. subtilis Hfq does not play a central role in post-transcriptional regulation but might have a more specialized function connected with stationary phase physiology. This would account for the high degree of conservation of Hfq proteins in all 17 B. subtilis strains whose genomes have been sequenced.</description><subject>Analysis</subject><subject>Bacillus subtilis</subject><subject>Bacillus subtilis - genetics</subject><subject>Bacillus subtilis - metabolism</subject><subject>Bacteria</subject><subject>Biology</subject><subject>Chemical treatment</subject><subject>Cholera</subject><subject>Conservation</subject><subject>Correlation analysis</subject><subject>Deletion mutant</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Fitness</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genetic engineering</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Gram-positive bacteria</subject><subject>Growth rate</subject><subject>Homeostasis</subject><subject>Host Factor 1 Protein - genetics</subject><subject>Host Factor 1 Protein - metabolism</subject><subject>Laboratories</subject><subject>Life Sciences</subject><subject>Organic chemistry</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Physiological aspects</subject><subject>Physiology</subject><subject>Post-transcription</subject><subject>Protein binding</subject><subject>Proteins</subject><subject>Regulatory mechanisms (biology)</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA-binding protein</subject><subject>Salmonella</subject><subject>Sporulation</subject><subject>Staphylococcus aureus</subject><subject>Stationary phase</subject><subject>Strain 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one</jtitle><addtitle>PLoS One</addtitle><date>2015-04-27</date><risdate>2015</risdate><volume>10</volume><issue>4</issue><spage>e0124977</spage><epage>e0124977</epage><pages>e0124977-e0124977</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>RNA-binding protein Hfq is a key component of the adaptive responses of many proteobacterial species including Escherichia coli, Salmonella enterica and Vibrio cholera. In these organisms, the importance of Hfq largely stems from its participation to regulatory mechanisms involving small non-coding RNAs. In contrast, the function of Hfq in Gram-positive bacteria has remained elusive and somewhat controversial. In the present study, we have further addressed this point by comparing growth phenotypes and transcription profiles between wild-type and an hfq deletion mutant of the model Gram-positive bacterium, Bacillus subtilis. The absence of Hfq had no significant consequences on growth rates under nearly two thousand metabolic conditions and chemical treatments. The only phenotypic difference was a survival defect of B. subtilis hfq mutant in rich medium in stationary phase. Transcriptomic analysis correlated this phenotype with a change in the levels of nearly one hundred transcripts. Albeit a significant fraction of these RNAs (36%) encoded sporulation-related functions, analyses in a strain unable to sporulate ruled out sporulation per se as the basis of the hfq mutant's stationary phase fitness defect. When expressed in Salmonella, B. subtilis hfq complemented the sharp loss of viability of a degP hfq double mutant, attenuating the chronic σE-activated phenotype of this strain. However, B. subtilis hfq did not complement other regulatory deficiencies resulting from loss of Hfq-dependent small RNA activity in Salmonella indicating a limited functional overlap between Salmonella and B. subtilis Hfqs. Overall, this study confirmed that, despite structural similarities with other Hfq proteins, B. subtilis Hfq does not play a central role in post-transcriptional regulation but might have a more specialized function connected with stationary phase physiology. This would account for the high degree of conservation of Hfq proteins in all 17 B. subtilis strains whose genomes have been sequenced.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25915524</pmid><doi>10.1371/journal.pone.0124977</doi><orcidid>https://orcid.org/0000-0003-3446-6987</orcidid><orcidid>https://orcid.org/0000-0002-4533-1220</orcidid><orcidid>https://orcid.org/0000-0003-4601-3387</orcidid><orcidid>https://orcid.org/0000-0002-7732-9491</orcidid><oa>free_for_read</oa></addata></record> |
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| language | eng |
| recordid | cdi_plos_journals_1676152141 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Analysis Bacillus subtilis Bacillus subtilis - genetics Bacillus subtilis - metabolism Bacteria Biology Chemical treatment Cholera Conservation Correlation analysis Deletion mutant E coli Escherichia coli Fitness Gene expression Gene regulation Genetic engineering Genomes Genomics Gram-positive bacteria Growth rate Homeostasis Host Factor 1 Protein - genetics Host Factor 1 Protein - metabolism Laboratories Life Sciences Organic chemistry Phenotype Phenotypes Physiological aspects Physiology Post-transcription Protein binding Proteins Regulatory mechanisms (biology) Ribonucleic acid RNA RNA-binding protein Salmonella Sporulation Staphylococcus aureus Stationary phase Strain analysis Studies Transcriptome Viability |
| title | Tracking the Elusive Function of Bacillus subtilis Hfq |
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