Transcriptional Attenuation Controls Macrolide Inducible Efflux and Resistance in Streptococcus pneumoniae and in Other Gram-Positive Bacteria Containing mef/mel(msr(D)) Elements

Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E...

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Published in:	PloS one Vol. 10; no. 2; p. e0116254
Main Authors:	Chancey, Scott T., Bai, Xianhe, Kumar, Nikhil, Drabek, Elliott F., Daugherty, Sean C., Colon, Thomas, Ott, Sandra, Sengamalay, Naomi, Sadzewicz, Lisa, Tallon, Luke J., Fraser, Claire M., Tettelin, Hervé, Stephens, David S.
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 19.02.2015 Public Library of Science (PLoS)
Subjects:	Anti-Bacterial Agents - pharmacology Antibiotics Attenuation Bacteria Bacterial infections Chromosomes Efflux Gene expression Genetic aspects Genomes Gram-positive bacteria Gram-Positive Bacteria - drug effects Guanine Infectious diseases Laboratories Laws, regulations and rules Macrolides - pharmacology Medicine Microbial drug resistance Microbial Sensitivity Tests mRNA stability Operons Pathogenesis Pneumonia Protein sorting signals Protein structure Purines Regulatory mechanisms (biology) Ribonucleic acid RNA Secondary structure Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - drug effects Streptococcus pyogenes Streptococcus pyogenes - drug effects Transcription Transcription (Genetics) Veterans Atlanta Georgia Georgia United States > US Maryland Baltimore Maryland
ISSN:	1932-6203, 1932-6203
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Abstract	Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E)/mel transcriptional start, localized the mef(E)/mel promoter, and demonstrated attenuation of transcription as a mechanism of regulation of macrolide-inducible mef-mediated macrolide resistance in S. pneumoniae. The mef(E)/mel transcriptional start site was a guanine 327 bp upstream of mef(E). Consensus pneumococcal promoter -10 (5'-TATACT-3') and -35 (5'-TTGAAC-3') boxes separated by 17 bp were identified 7 bp upstream of the start site. Analysis of the predicted secondary structure of the 327 5' region identified four pairs of inverted repeats R1-R8 predicted to fold into stem-loops, a small leader peptide [MTASMRLR, (Mef(E)L)] required for macrolide induction and a Rho-independent transcription terminator. RNA-seq analyses provided confirmation of transcriptional attenuation. In addition, expression of mef(E)L was also influenced by mef(E)L-dependent mRNA stability. The regulatory region 5' of mef(E) was highly conserved in other mef/mel(msr)-containing elements including Tn1207.1 and the 5612IQ complex in pneumococci and Tn1207.3 in Group A streptococci, indicating a regulatory mechanism common to a wide variety of Gram-positive bacteria containing mef/mel(msr) elements.
AbstractList	Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E)/mel transcriptional start, localized the mef(E)/mel promoter, and demonstrated attenuation of transcription as a mechanism of regulation of macrolide-inducible mef-mediated macrolide resistance in S. pneumoniae. The mef(E)/mel transcriptional start site was a guanine 327 bp upstream of mef(E). Consensus pneumococcal promoter -10 (5′-TATACT-3′) and -35 (5′-TTGAAC-3′) boxes separated by 17 bp were identified 7 bp upstream of the start site. Analysis of the predicted secondary structure of the 327 5’ region identified four pairs of inverted repeats R1-R8 predicted to fold into stem-loops, a small leader peptide [MTASMRLR, (Mef(E)L)] required for macrolide induction and a Rho-independent transcription terminator. RNA-seq analyses provided confirmation of transcriptional attenuation. In addition, expression of mef(E)L was also influenced by mef(E)L-dependent mRNA stability. The regulatory region 5’ of mef(E) was highly conserved in other mef/mel(msr)-containing elements including Tn1207.1 and the 5612IQ complex in pneumococci and Tn1207.3 in Group A streptococci, indicating a regulatory mechanism common to a wide variety of Gram-positive bacteria containing mef/mel(msr) elements. Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E)/mel transcriptional start, localized the mef(E)/mel promoter, and demonstrated attenuation of transcription as a mechanism of regulation of macrolide-inducible mef-mediated macrolide resistance in S. pneumoniae. The mef(E)/mel transcriptional start site was a guanine 327 bp upstream of mef(E). Consensus pneumococcal promoter -10 (5'-TATACT-3') and -35 (5'-TTGAAC-3') boxes separated by 17 bp were identified 7 bp upstream of the start site. Analysis of the predicted secondary structure of the 327 5' region identified four pairs of inverted repeats R1-R8 predicted to fold into stem-loops, a small leader peptide [MTASMRLR, (Mef(E)L)] required for macrolide induction and a Rho-independent transcription terminator. RNA-seq analyses provided confirmation of transcriptional attenuation. In addition, expression of mef(E)L was also influenced by mef(E)L-dependent mRNA stability. The regulatory region 5' of mef(E) was highly conserved in other mef/mel(msr)-containing elements including Tn1207.1 and the 5612IQ complex in pneumococci and Tn1207.3 in Group A streptococci, indicating a regulatory mechanism common to a wide variety of Gram-positive bacteria containing mef/mel(msr) elements.Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E)/mel transcriptional start, localized the mef(E)/mel promoter, and demonstrated attenuation of transcription as a mechanism of regulation of macrolide-inducible mef-mediated macrolide resistance in S. pneumoniae. The mef(E)/mel transcriptional start site was a guanine 327 bp upstream of mef(E). Consensus pneumococcal promoter -10 (5'-TATACT-3') and -35 (5'-TTGAAC-3') boxes separated by 17 bp were identified 7 bp upstream of the start site. Analysis of the predicted secondary structure of the 327 5' region identified four pairs of inverted repeats R1-R8 predicted to fold into stem-loops, a small leader peptide [MTASMRLR, (Mef(E)L)] required for macrolide induction and a Rho-independent transcription terminator. RNA-seq analyses provided confirmation of transcriptional attenuation. In addition, expression of mef(E)L was also influenced by mef(E)L-dependent mRNA stability. The regulatory region 5' of mef(E) was highly conserved in other mef/mel(msr)-containing elements including Tn1207.1 and the 5612IQ complex in pneumococci and Tn1207.3 in Group A streptococci, indicating a regulatory mechanism common to a wide variety of Gram-positive bacteria containing mef/mel(msr) elements. Macrolide resistance, emerging in Streptococcus pneumoniae and other Gram-positive bacteria, is increasingly due to efflux pumps encoded by mef/mel(msr) operons found on discrete mobile genetic elements. The regulation of mef/mel(msr) in these elements is not well understood. We identified the mef(E)/mel transcriptional start, localized the mef(E)/mel promoter, and demonstrated attenuation of transcription as a mechanism of regulation of macrolide-inducible mef -mediated macrolide resistance in S . pneumoniae . The mef(E)/mel transcriptional start site was a guanine 327 bp upstream of mef(E) . Consensus pneumococcal promoter -10 (5′-TATACT-3′) and -35 (5′-TTGAAC-3′) boxes separated by 17 bp were identified 7 bp upstream of the start site. Analysis of the predicted secondary structure of the 327 5’ region identified four pairs of inverted repeats R1-R8 predicted to fold into stem-loops, a small leader peptide [MTASMRLR, (Mef(E)L)] required for macrolide induction and a Rho-independent transcription terminator. RNA-seq analyses provided confirmation of transcriptional attenuation. In addition, expression of mef(E)L was also influenced by mef(E)L -dependent mRNA stability. The regulatory region 5’ of mef(E) was highly conserved in other mef/mel(msr) -containing elements including Tn 1207.1 and the 5612IQ complex in pneumococci and Tn 1207.3 in Group A streptococci, indicating a regulatory mechanism common to a wide variety of Gram-positive bacteria containing mef/mel(msr) elements.
Audience	Academic
Author	Fraser, Claire M. Drabek, Elliott F. Kumar, Nikhil Chancey, Scott T. Tettelin, Hervé Bai, Xianhe Ott, Sandra Daugherty, Sean C. Sadzewicz, Lisa Tallon, Luke J. Sengamalay, Naomi Colon, Thomas Stephens, David S.
AuthorAffiliation	University of Kansas Medical Center, UNITED STATES 5 Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America 2 Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center, Atlanta, Georgia, United States of America 3 Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America 4 Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, United States of America 1 Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia, United States of America
AuthorAffiliation_xml	– name: 2 Laboratories of Microbial Pathogenesis, Department of Veterans Affairs Medical Center, Atlanta, Georgia, United States of America – name: 5 Department of Microbiology and Immunology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America – name: University of Kansas Medical Center, UNITED STATES – name: 3 Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, United States of America – name: 1 Division of Infectious Diseases, Department of Medicine, Emory University School of Medicine, Atlanta, Georgia, United States of America – name: 4 Department of Medicine, University of Maryland School of Medicine, Baltimore, Maryland, United States of America
Author_xml	– sequence: 1 givenname: Scott T. surname: Chancey fullname: Chancey, Scott T. – sequence: 2 givenname: Xianhe surname: Bai fullname: Bai, Xianhe – sequence: 3 givenname: Nikhil surname: Kumar fullname: Kumar, Nikhil – sequence: 4 givenname: Elliott F. surname: Drabek fullname: Drabek, Elliott F. – sequence: 5 givenname: Sean C. surname: Daugherty fullname: Daugherty, Sean C. – sequence: 6 givenname: Thomas surname: Colon fullname: Colon, Thomas – sequence: 7 givenname: Sandra surname: Ott fullname: Ott, Sandra – sequence: 8 givenname: Naomi surname: Sengamalay fullname: Sengamalay, Naomi – sequence: 9 givenname: Lisa surname: Sadzewicz fullname: Sadzewicz, Lisa – sequence: 10 givenname: Luke J. surname: Tallon fullname: Tallon, Luke J. – sequence: 11 givenname: Claire M. surname: Fraser fullname: Fraser, Claire M. – sequence: 12 givenname: Hervé surname: Tettelin fullname: Tettelin, Hervé – sequence: 13 givenname: David S. surname: Stephens fullname: Stephens, David S.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25695510$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: STC DSS. Performed the experiments: STC XB NK NS LS LJT TC SO. Analyzed the data: STC SD EFD HT DSS. Wrote the paper: STC HT DSS. Supervised sequencing and analysis activities: CMF.
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SubjectTerms	Anti-Bacterial Agents - pharmacology Antibiotics Attenuation Bacteria Bacterial infections Chromosomes Efflux Gene expression Genetic aspects Genomes Gram-positive bacteria Gram-Positive Bacteria - drug effects Guanine Infectious diseases Laboratories Laws, regulations and rules Macrolides - pharmacology Medicine Microbial drug resistance Microbial Sensitivity Tests mRNA stability Operons Pathogenesis Pneumonia Protein sorting signals Protein structure Purines Regulatory mechanisms (biology) Ribonucleic acid RNA Secondary structure Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - drug effects Streptococcus pyogenes Streptococcus pyogenes - drug effects Transcription Transcription (Genetics) Veterans
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Title	Transcriptional Attenuation Controls Macrolide Inducible Efflux and Resistance in Streptococcus pneumoniae and in Other Gram-Positive Bacteria Containing mef/mel(msr(D)) Elements
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