Methionine-mediated gene expression and characterization of the CmhR regulon in Streptococcus pneumoniae

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Abstract

This study investigated the transcriptomic response of Streptococcus pneumoniae D39 to methionine. Transcriptome comparison of the S. pneumoniae D39 wild-type grown in chemically defined medium with 0–10 mM methionine revealed the elevated expression of various genes/operons involved in methionine synthesis and transport ( fhs, folD, gshT, metA, metB-csd, metEF, metQ, tcyB, spd-0150, spd-0431 and spd-0618). Furthermore, β-galactosidase assays and quantitative RT-PCR studies demonstrated that the transcriptional regulator, CmhR (SPD-0588), acts as a transcriptional activator of the fhs, folD, metB-csd, metEF, metQ and spd-0431 genes. A putative regulatory site of CmhR was identified in the promoter region of CmhR-regulated genes and this CmhR site was further confirmed by promoter mutational experiments.

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Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6.

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Streptococcus pneumoniae (pneumococcus) is a leading human respiratory pathogen that causes a variety of serious mucosal and invasive diseases. D39 is an historically important serotype 2 strain that was used in experiments by Avery and coworkers to demonstrate that DNA is the genetic material. Although isolated nearly a century ago, D39 remains extremely virulent in murine infection models and is perhaps the strain used most frequently in current studies of pneumococcal pathogenesis. To date, the complete genome sequences have been reported for only two S. pneumoniae strains: TIGR4, a recent serotype 4 clinical isolate, and laboratory strain R6, an avirulent, unencapsulated derivative of strain D39. We report here the genome sequences and new annotation of two different isolates of strain D39 and the corrected sequence of strain R6. Comparisons of these three related sequences allowed deduction of the likely sequence of the D39 progenitor and mutations that arose in each isolate. Despite its numerous repeated sequences and IS elements, the serotype 2 genome has remained remarkably stable during cultivation, and one of the D39 isolates contains only five relatively minor mutations compared to the deduced D39 progenitor. In contrast, laboratory strain R6 contains 71 single-base-pair changes, six deletions, and four insertions and has lost the cryptic pDP1 plasmid compared to the D39 progenitor strain. Many of these mutations are in or affect the expression of genes that play important roles in regulation, metabolism, and virulence. The nature of the mutations that arose spontaneously in these three strains, the relative global transcription patterns determined by microarray analyses, and the implications of the D39 genome sequences to studies of pneumococcal physiology and pathogenesis are presented and discussed.

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Author and article information

Journal

Journal ID (nlm-ta): Microb Genom

Journal ID (publisher-id): MGen

Title: Microbial Genomics

Publisher: Microbiology Society

ISSN (Electronic): 2057-5858

Publication date Collection: October 2016

Publication date (Electronic): 21 October 2016

Volume: 2

Issue: 10

Electronic Location Identifier: e000091

Affiliations

[ ¹ ]Department of Molecular Genetics, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen , Nijenborgh 7, 9747 AG, Groningen, The Netherlands

[ ² ]Department of Bioinformatics and Biotechnology, G C University , Faisalabad, Pakistan

[ ³ ]Department of Microbiology, Tumor and Cell Biology, , Karolinska Institutet , Nobels väg 16, Stockholm, SE-171 77, Sweden

Author notes

Correspondence Oscar P. Kuipers ( o.p.kuipers@ 123456rug.nl )

All supporting data, code and protocols have been provided within the article or through supplementary data files.

Article

Publisher ID: mgen000091

DOI: 10.1099/mgen.0.000091

PMC ID: 5359408

PubMed ID: 28348831

SO-VID: 5de4895c-e8ac-4efe-8223-a3c9e7368e15

License:

This is an open access article under the terms of the Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.