The Impact of 18 Ancestral and Horizontally-Acquired Regulatory Proteins upon the Transcriptome and sRNA Landscape of Salmonella enterica serovar Typhimurium
We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcr...
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| Published in | PLoS genetics Vol. 12; no. 8; p. e1006258 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
26.08.2016
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS (σ38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. |
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| AbstractList | We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS (σ38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS ([sigma].sup.38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS ([sigma]38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS ([sigma]38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S . Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS (σ 38 ) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. The transcriptional networks and the functions of small regulatory RNAs of Salmonella enterica serovar Typhimurium are being studied intensively. S . Typhimurium is becoming the ideal model pathogen for linking transcriptional and post-transcriptional gene regulation to bacterial virulence. Here, we systematically defined the regulatory factors responsible for controlling the expression of S . Typhimurium coding genes and sRNAs under infection-relevant growth conditions. As well as confirming published regulatory inputs for Salmonella pathogenicity islands, such as the positive role played by Fur in the expression of SPI1, we report, for the first time, the global impact of the FliZ, HilE and PhoB/R transcription factors and identify 124 sRNAs that belong to virulence-associated regulons. We found a subset of genes of known and unknown function that are regulated by both HilD and SsrB, highlighting the cross-talk mechanisms that control Salmonella virulence. An integrative analysis of the regulatory datasets revealed 5 coding genes of unknown function that may play novel roles in virulence. We hope that the SalComRegulon resource will be a dynamic database that will be constantly updated to inspire new hypothesis-driven experimentation, and will contribute to the construction of a comprehensive transcriptional network for S . Typhimurium. We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS (σ38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon.We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene regulation. New tools for studying transcripts at the single nucleotide level now offer an unparalleled opportunity to understand the bacterial transcriptome, and expression of the small RNAs (sRNA) and coding genes responsible for the establishment of infection. Here, we define the transcriptomes of 18 mutants lacking virulence-related global regulatory systems that modulate the expression of the SPI1 and SPI2 Type 3 secretion systems of S. Typhimurium strain 4/74. Using infection-relevant growth conditions, we identified a total of 1257 coding genes that are controlled by one or more regulatory system, including a sub-class of genes that reflect a new level of cross-talk between SPI1 and SPI2. We directly compared the roles played by the major transcriptional regulators in the expression of sRNAs, and discovered that the RpoS (σ38) sigma factor modulates the expression of 23% of sRNAs, many more than other regulatory systems. The impact of the RNA chaperone Hfq upon the steady state levels of 280 sRNA transcripts is described, and we found 13 sRNAs that are co-regulated with SPI1 and SPI2 virulence genes. We report the first example of an sRNA, STnc1480, that is subject to silencing by H-NS and subsequent counter-silencing by PhoP and SlyA. The data for these 18 regulatory systems is now available to the bacterial research community in a user-friendly online resource, SalComRegulon. |
| Audience | Academic |
| Author | Hokamp, Karsten Diard, Médéric Sivasankaran, Sathesh K. Hinton, Jay C. D. Puente, José L. Colgan, Aoife M. Kröger, Carsten Hardt, Wolf-Dietrich |
| AuthorAffiliation | 4 Department of Genetics, School of Genetics and Microbiology, Smurfit Institute of Genetics, Trinity College, Dublin, Ireland 5 Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom Universidad de Sevilla, SPAIN 3 Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de Mexico, Cuernavaca, Morelos, Mexico 1 Department of Microbiology, School of Genetics and Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin, Ireland 2 Institute of Microbiology, ETH Zürich, Zürich, Switzerland |
| AuthorAffiliation_xml | – name: 3 Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de Mexico, Cuernavaca, Morelos, Mexico – name: 4 Department of Genetics, School of Genetics and Microbiology, Smurfit Institute of Genetics, Trinity College, Dublin, Ireland – name: 1 Department of Microbiology, School of Genetics and Microbiology, Moyne Institute of Preventive Medicine, Trinity College, Dublin, Ireland – name: 2 Institute of Microbiology, ETH Zürich, Zürich, Switzerland – name: 5 Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom – name: Universidad de Sevilla, SPAIN |
| Author_xml | – sequence: 1 givenname: Aoife M. surname: Colgan fullname: Colgan, Aoife M. – sequence: 2 givenname: Carsten orcidid: 0000-0003-0461-1530 surname: Kröger fullname: Kröger, Carsten – sequence: 3 givenname: Médéric surname: Diard fullname: Diard, Médéric – sequence: 4 givenname: Wolf-Dietrich surname: Hardt fullname: Hardt, Wolf-Dietrich – sequence: 5 givenname: José L. surname: Puente fullname: Puente, José L. – sequence: 6 givenname: Sathesh K. surname: Sivasankaran fullname: Sivasankaran, Sathesh K. – sequence: 7 givenname: Karsten surname: Hokamp fullname: Hokamp, Karsten – sequence: 8 givenname: Jay C. D. surname: Hinton fullname: Hinton, Jay C. D. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27564394$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2016 Public Library of Science 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: serovar Typhimurium. PLoS Genet 12(8): e1006258. doi:10.1371/journal.pgen.1006258 2016 Colgan et al 2016 Colgan et al 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: serovar Typhimurium. PLoS Genet 12(8): e1006258. doi:10.1371/journal.pgen.1006258 |
| Copyright_xml | – notice: COPYRIGHT 2016 Public Library of Science – notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: serovar Typhimurium. PLoS Genet 12(8): e1006258. doi:10.1371/journal.pgen.1006258 – notice: 2016 Colgan et al 2016 Colgan et al – notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: serovar Typhimurium. PLoS Genet 12(8): e1006258. doi:10.1371/journal.pgen.1006258 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: AMC CK MD WDH JLP JCDH.Performed the experiments: AMC CK.Analyzed the data: AMC CK JLP JCDH.Contributed reagents/materials/analysis tools: MD WDH SKS KH.Wrote the paper: AMC CK MD WDH JLP SKS KH JCDH. The authors have declared that no competing interests exist. |
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| Snippet | We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene... We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene... We know a great deal about the genes used by the model pathogen Salmonella enterica serovar Typhimurium to cause disease, but less about global gene... |
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| SubjectTerms | Bacterial Proteins - biosynthesis Bacterial Proteins - genetics Biology and Life Sciences Datasets Deoxyribonucleic acid DNA Experiments Gene expression Gene Expression Regulation, Bacterial Genetic aspects Genetic regulation Genetic research Genetic testing Host Factor 1 Protein - biosynthesis Host Factor 1 Protein - genetics Infections Mammals Medicine and Health Sciences Membrane Proteins - biosynthesis Membrane Proteins - genetics Mortality Pathogens Phylogenetics RNA RNA, Small Untranslated - genetics Salmonella Salmonella enterica Salmonella typhimurium Salmonella typhimurium - genetics Salmonella typhimurium - growth & development Salmonella typhimurium - pathogenicity Serogroup Sigma Factor - biosynthesis Sigma Factor - genetics Transcription factors Transcriptome - genetics Virulence |
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| Title | The Impact of 18 Ancestral and Horizontally-Acquired Regulatory Proteins upon the Transcriptome and sRNA Landscape of Salmonella enterica serovar Typhimurium |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/27564394 https://www.proquest.com/docview/1820285424 https://www.proquest.com/docview/1815365056 https://www.proquest.com/docview/1827895546 https://pubmed.ncbi.nlm.nih.gov/PMC5001712 https://doaj.org/article/cd1762815379418b9b9160edf9ccea38 http://dx.doi.org/10.1371/journal.pgen.1006258 |
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