{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T23:11:36Z","timestamp":1791155496553,"version":"4.1.0"},"reference-count":60,"publisher":"Microbiology Society","issue":"12","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2009,12,1]]},"abstract":"<jats:p><jats:italic>Streptococcus pneumoniae<\/jats:italic>resides in the oxygen-rich environment of the upper respiratory tract, and therefore the ability to survive in the presence of oxygen is an important aspect of its<jats:italic>in vivo<\/jats:italic>survival. To investigate how<jats:italic>S. pneumoniae<\/jats:italic>adapts to oxygen, we determined the global gene expression profile of the micro-organism in aerobiosis and anaerobiosis. It was found that exposure to aerobiosis elevated the expression of 54 genes, while the expression of 15 genes was downregulated. Notably there were significant changes in putative genome plasticity and hypothetical genes. In addition, increased expression of<jats:italic>rgg<\/jats:italic>, a putative transcriptional regulator, was detected. To test the role of Rgg in the pneumococcal oxidative stress response, an isogenic mutant was constructed. It was found that the mutant was sensitive to oxygen and paraquat, but not to H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub>. In addition, the absence of Rgg strongly reduced the biofilm-forming ability of an unencapsulated pneumococcus. Virulence studies showed that the median survival time of mice infected intranasally with the<jats:italic>rgg<\/jats:italic>mutant was significantly longer than that of the wild-type-infected group, and the animals infected with the mutant developed septicaemia later than those infected intranasally with the wild-type.<\/jats:p>","DOI":"10.1099\/mic.0.028282-0","type":"journal-article","created":{"date-parts":[[2009,11,3]],"date-time":"2009-11-03T22:52:21Z","timestamp":1257288741000},"page":"4123-4134","source":"Crossref","is-referenced-by-count":52,"title":["The pneumococcal response to oxidative stress includes a role for Rgg"],"prefix":"10.1099","volume":"155","author":[{"given":"Magda E.","family":"Bortoni","sequence":"first","affiliation":[{"name":"Department of Basic Sciences, Universidad De Monterrey, Monterrey 66238, Mexico"},{"name":"Department of Infection, Immunity and Inflammation, University of Leicester, Leicester LE1 9HN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vanessa S.","family":"Terra","sequence":"additional","affiliation":[{"name":"Department of Infection, Immunity and Inflammation, University of Leicester, Leicester LE1 9HN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason","family":"Hinds","sequence":"additional","affiliation":[{"name":"Division of Cellular and Molecular Medicine, St George's Hospital Medical School, University of London, London SW17 0RE, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter W.","family":"Andrew","sequence":"additional","affiliation":[{"name":"Department of Infection, Immunity and Inflammation, University of Leicester, Leicester LE1 9HN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hasan","family":"Yesilkaya","sequence":"additional","affiliation":[{"name":"Department of Infection, Immunity and Inflammation, University of Leicester, Leicester LE1 9HN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"R1","doi-asserted-by":"crossref","first-page":"3748","DOI":"10.1128\/JB.00169-06","article-title":"Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans","volume":"188","author":"Abranches","year":"2006","journal-title":"J Bacteriol"},{"key":"R2","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1111\/j.1365-2958.1996.tb02556.x","article-title":"Competence pheromone, oligopeptide permease, and induction of competence in Streptococcus pneumoniae","volume":"21","author":"Alloing","year":"1996","journal-title":"Mol Microbiol"},{"key":"R3","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.mib.2005.02.014","article-title":"The bgl sensory system: a transmembrane signaling pathway controlling transcriptional antitermination","volume":"8","author":"Amster-Choder","year":"2005","journal-title":"Curr Opin Microbiol"},{"key":"R4","doi-asserted-by":"crossref","first-page":"5621","DOI":"10.1128\/JB.179.17.5621-5624.1997","article-title":"BglG, the response regulator of the Escherichia coli bgl operon, is phosphorylated on a histidine residue","volume":"179","author":"Amster-Choder","year":"1997","journal-title":"J Bacteriol"},{"key":"R5","doi-asserted-by":"crossref","first-page":"5279","DOI":"10.1128\/JB.00100-08","article-title":"The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities","volume":"190","author":"Atack","year":"2008","journal-title":"J Bacteriol"},{"key":"R6","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1046\/j.1365-2958.1999.01663.x","article-title":"The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence","volume":"34","author":"Auzat","year":"1999","journal-title":"Mol Microbiol"},{"key":"R7","doi-asserted-by":"crossref","first-page":"8769","DOI":"10.1074\/jbc.M312388200","article-title":"Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth","volume":"279","author":"Cha","year":"2004","journal-title":"J Biol Chem"},{"key":"R8","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1186\/1471-2164-6-115","article-title":"Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide","volume":"6","author":"Chang","year":"2005","journal-title":"BMC Genomics"},{"key":"R9","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1128\/JB.188.4.1648-1659.2006","article-title":"Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide","volume":"188","author":"Chang","year":"2006","journal-title":"J Bacteriol"},{"key":"R10","doi-asserted-by":"crossref","first-page":"6016","DOI":"10.1128\/JB.185.20.6016-6024.2003","article-title":"Rgg coordinates virulence factor synthesis and metabolism in Streptococcus pyogenes","volume":"185","author":"Chaussee","year":"2003","journal-title":"J Bacteriol"},{"key":"R11","doi-asserted-by":"crossref","first-page":"7091","DOI":"10.1128\/JB.186.21.7091-7099.2004","article-title":"Rgg regulates growth phase-dependent expression of proteins associated with secondary metabolism and stress in Streptococcus pyogenes","volume":"186","author":"Chaussee","year":"2004","journal-title":"J Bacteriol"},{"key":"R12","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1078\/1438-4221-00139","article-title":"Pathogenicity of Legionella pneumophila","volume":"291","author":"Cianciotto","year":"2001","journal-title":"Int J Med Microbiol"},{"key":"R13","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1111\/j.1365-2958.2003.03892.x","article-title":"Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells","volume":"51","author":"Dagkessamanskaia","year":"2004","journal-title":"Mol Microbiol"},{"key":"R14","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1111\/j.1574-6968.2008.01171.x","article-title":"Inter- and intraserotypic variation in the Streptococcus pyogenes Rgg regulon","volume":"284","author":"Dmitriev","year":"2008","journal-title":"FEMS Microbiol Lett"},{"key":"R15","doi-asserted-by":"crossref","first-page":"4599","DOI":"10.1128\/JB.183.15.4599-4608.2001","article-title":"Competence repression under oxygen limitation through the two-component MicAB signal-transducing system in Streptococcus pneumoniae and involvement of the PAS domain of MicB","volume":"183","author":"Echenique","year":"2001","journal-title":"J Bacteriol"},{"key":"R16","doi-asserted-by":"crossref","first-page":"688","DOI":"10.1046\/j.1365-2958.2000.01891.x","article-title":"Competence regulation by oxygen in Streptococcus pneumoniae: involvement of ciaRH and comCDE","volume":"36","author":"Echenique","year":"2000","journal-title":"Mol Microbiol"},{"key":"R17","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1196\/annals.1391.008","article-title":"Review on bacterial stress topics","author":"Giuliodori","year":"2007","journal-title":"Ann N Y Acad Sci"},{"key":"R18","doi-asserted-by":"crossref","first-page":"Article27","DOI":"10.2202\/1544-6115.1302","article-title":"On the operational characteristics of the Benjamini and Hochberg false discovery rate procedure","volume":"6","author":"Green","year":"2007","journal-title":"Stat Appl Genet Mol Biol"},{"key":"R19","first-page":"528","article-title":"Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction","volume":"8","author":"Horton","year":"1990","journal-title":"Biotechniques"},{"key":"R20","doi-asserted-by":"crossref","first-page":"5709","DOI":"10.1128\/JB.183.19.5709-5717.2001","article-title":"Genome of the bacterium Streptococcus pneumoniae strain R6","volume":"183","author":"Hoskins","year":"2001","journal-title":"J Bacteriol"},{"key":"R21","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1128\/JB.01410-07","article-title":"A novel role for enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm","volume":"190","author":"Houot","year":"2008","journal-title":"J Bacteriol"},{"key":"R22","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1038\/nrmicro1871","article-title":"The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease","volume":"6","author":"Kadioglu","year":"2008","journal-title":"Nat Rev Microbiol"},{"key":"R23","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/S0966-842X(03)00098-2","article-title":"Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen\u2013host interactions","volume":"11","author":"Kreikemeyer","year":"2003","journal-title":"Trends Microbiol"},{"key":"R24","doi-asserted-by":"crossref","first-page":"5470","DOI":"10.1002\/j.1460-2075.1996.tb00930.x","article-title":"A purified mariner transposase is sufficient to mediate transposition in vitro","volume":"15","author":"Lampe","year":"1996","journal-title":"EMBO J"},{"key":"R25","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1128\/JB.01148-06","article-title":"Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6","volume":"189","author":"Lanie","year":"2007","journal-title":"J Bacteriol"},{"key":"R26","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2\u2212\u0394\u0394CT method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"R27","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1046\/j.1365-2958.2000.02187.x","article-title":"Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae","volume":"38","author":"Martin","year":"2000","journal-title":"Mol Microbiol"},{"key":"R28","doi-asserted-by":"crossref","first-page":"3935","DOI":"10.1099\/mic.0.28238-0","article-title":"Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae","volume":"151","author":"Martin-Galiano","year":"2005","journal-title":"Microbiology"},{"key":"R29","doi-asserted-by":"crossref","first-page":"1661","DOI":"10.1111\/j.1365-2958.2003.03917.x","article-title":"A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae","volume":"51","author":"McCluskey","year":"2004","journal-title":"Mol Microbiol"},{"key":"R30","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1023\/A:1020540503200","article-title":"Defences against oxidative stress during starvation in bacteria","volume":"81","author":"McDougald","year":"2002","journal-title":"Antonie Van Leeuwenhoek"},{"key":"R31","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1046\/j.1365-2958.2002.03015.x","article-title":"Regulation of inducible peroxide stress responses","volume":"45","author":"Mongkolsuk","year":"2002","journal-title":"Mol Microbiol"},{"key":"R32","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1038\/317106a0","article-title":"Pain and laboratory animals","volume":"317","author":"Morton","year":"1985","journal-title":"Nature"},{"key":"R33","doi-asserted-by":"crossref","first-page":"7785","DOI":"10.1128\/JB.00673-06","article-title":"Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion","volume":"188","author":"Moscoso","year":"2006","journal-title":"J Bacteriol"},{"key":"R34","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1099\/mic.0.26665-0","article-title":"Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress","volume":"150","author":"Mostertz","year":"2004","journal-title":"Microbiology"},{"key":"R35","doi-asserted-by":"crossref","first-page":"5049","DOI":"10.1128\/IAI.00425-08","article-title":"Isolation of Streptococcus pneumoniae biofilm mutants and their characterization during nasopharyngeal colonization","volume":"76","author":"Mun\u0303oz-Eli\u0301as","year":"2008","journal-title":"Infect Immun"},{"key":"R36","first-page":"531","article-title":"Overview on sugar metabolism and its control in Lactococcus lactis \u2013 the input from in vivo NMR","volume":"29","author":"Neves","year":"2005","journal-title":"FEMS Microbiol Rev"},{"key":"R37","doi-asserted-by":"crossref","first-page":"1196","DOI":"10.1111\/j.1365-2958.2006.05310.x","article-title":"Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis","volume":"61","author":"Oggioni","year":"2006","journal-title":"Mol Microbiol"},{"key":"R38","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1128\/JB.184.9.2344-2351.2002","article-title":"Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK","volume":"184","author":"Ogura","year":"2002","journal-title":"J Bacteriol"},{"key":"R39","doi-asserted-by":"crossref","first-page":"5582","DOI":"10.1128\/IAI.72.10.5582-5596.2004","article-title":"Microarray analysis of pneumococcal gene expression during invasive disease","volume":"72","author":"Orihuela","year":"2004","journal-title":"Infect Immun"},{"key":"R40","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.micpath.2005.12.003","article-title":"An operon in Streptococcus pneumoniae containing a putative alkylhydroperoxidase D homologue contributes to virulence and the response to oxidative stress","volume":"40","author":"Paterson","year":"2006","journal-title":"Microb Pathog"},{"key":"R41","doi-asserted-by":"crossref","first-page":"6815","DOI":"10.1128\/JB.185.23.6815-6825.2003","article-title":"Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction","volume":"185","author":"Pericone","year":"2003","journal-title":"J Bacteriol"},{"key":"R42","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.bbamem.2006.12.016","article-title":"Effect of hydrogen peroxide production and the Fenton reaction on membrane composition of Streptococcus pneumoniae","volume":"1768","author":"Pesakhov","year":"2007","journal-title":"Biochim Biophys Acta"},{"key":"R43","doi-asserted-by":"crossref","first-page":"2701","DOI":"10.1128\/JB.180.10.2701-2710.1998","article-title":"Isolation and characterization of three Streptococcus pneumoniae transformation-specific loci by use of a lacZ reporter insertion vector","volume":"180","author":"Pestova","year":"1998","journal-title":"J Bacteriol"},{"key":"R44","doi-asserted-by":"crossref","first-page":"3225","DOI":"10.1128\/JB.01843-07","article-title":"Deficiency of the Rgg regulator promotes H2O2 resistance, AhpCF-mediated H2O2 decomposition, and virulence in Streptococcus pyogenes","volume":"190","author":"Pulliainen","year":"2008","journal-title":"J Bacteriol"},{"key":"R45","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1046\/j.1365-2958.2000.01931.x","article-title":"Global analysis of transcription kinetics during competence development in Streptococcus pneumoniae using high density DNA arrays","volume":"36","author":"Rimini","year":"2000","journal-title":"Mol Microbiol"},{"key":"R46","doi-asserted-by":"crossref","first-page":"6895","DOI":"10.1128\/JB.178.23.6895-6903.1996","article-title":"Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide","volume":"178","author":"Rocha","year":"1996","journal-title":"J Bacteriol"},{"key":"R47","doi-asserted-by":"crossref","first-page":"5625","DOI":"10.1128\/IAI.00667-06","article-title":"The transcriptional regulator RovS controls the attachment of Streptococcus agalactiae to human epithelial cells and the expression of virulence genes","volume":"74","author":"Samen","year":"2006","journal-title":"Infect Immun"},{"key":"R48","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1093\/genetics\/50.1.31","article-title":"A new synthetic medium for Diplococcus pneumoniae, and its use for the study of reciprocal transformations at the amiA locus","volume":"50","author":"Sicard","year":"1964","journal-title":"Genetics"},{"key":"R49","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1046\/j.1365-2958.1996.425954.x","article-title":"Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae","volume":"19","author":"Spellerberg","year":"1996","journal-title":"Mol Microbiol"},{"key":"R50","doi-asserted-by":"crossref","first-page":"3129","DOI":"10.1099\/00221287-148-10-3129","article-title":"Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays","volume":"148","author":"Stewart","year":"2002","journal-title":"Microbiology"},{"key":"R51","doi-asserted-by":"crossref","first-page":"12391","DOI":"10.1073\/pnas.182380799","article-title":"Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae","volume":"99","author":"Tettelin","year":"2002","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R52","doi-asserted-by":"crossref","first-page":"33488","DOI":"10.1074\/jbc.M103743200","article-title":"The anaerobic ribonucleotide reductase from Lactococcus lactis. Interactions between the two proteins NrdD and NrdG","volume":"276","author":"Torrents","year":"2001","journal-title":"J Biol Chem"},{"key":"R53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1006\/abbi.1999.1518","article-title":"Iron and oxidative stress in bacteria","volume":"373","author":"Touati","year":"2000","journal-title":"Arch Biochem Biophys"},{"key":"R54","doi-asserted-by":"crossref","first-page":"1635","DOI":"10.1128\/IAI.70.3.1635-1639.2002","article-title":"Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress","volume":"70","author":"Tseng","year":"2002","journal-title":"Infect Immun"},{"key":"R55","doi-asserted-by":"crossref","first-page":"8123","DOI":"10.1128\/JB.186.23.8123-8136.2004","article-title":"Regulation of iron transport in Streptococcus pneumoniae by RitR, an orphan response regulator","volume":"186","author":"Ulijasz","year":"2004","journal-title":"J Bacteriol"},{"key":"R56","doi-asserted-by":"crossref","first-page":"5555","DOI":"10.1128\/JB.185.18.5555-5562.2003","article-title":"Glutathione and catalase provide overlapping defenses for protection against respiration-generated hydrogen peroxide in Haemophilus influenzae","volume":"185","author":"Vergauwen","year":"2003","journal-title":"J Bacteriol"},{"key":"R57","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1099\/mic.0.25983-0","article-title":"An amino acid change near the carboxyl terminus of the Streptococcus gordonii regulatory protein Rgg affects its abilities to bind DNA and influence expression of the glucosyltransferase gene gtfG","volume":"149","author":"Vickerman","year":"2003","journal-title":"Microbiology"},{"key":"R58","doi-asserted-by":"crossref","first-page":"5430","DOI":"10.1128\/IAI.69.9.5430-5439.2001","article-title":"Changes in availability of oxygen accentuate differences in capsular polysaccharide expression by phenotypic variants and clinical isolates of Streptococcus pneumoniae","volume":"69","author":"Weiser","year":"2001","journal-title":"Infect Immun"},{"key":"R59","doi-asserted-by":"crossref","first-page":"2819","DOI":"10.1128\/IAI.68.5.2819-2826.2000","article-title":"Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae","volume":"68","author":"Yesilkaya","year":"2000","journal-title":"Infect Immun"},{"key":"R60","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.tube.2005.08.019","article-title":"The genetic portrait of an outbreak strain","volume":"86","author":"Yesilkaya","year":"2006","journal-title":"Tuberculosis"}],"container-title":["Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.028282-0?crawler=true","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,13]],"date-time":"2021-10-13T09:27:45Z","timestamp":1634117265000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/micro\/10.1099\/mic.0.028282-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,12,1]]},"references-count":60,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2009,12,1]]}},"URL":"https:\/\/doi.org\/10.1099\/mic.0.028282-0","relation":{},"ISSN":["1350-0872","1465-2080"],"issn-type":[{"value":"1350-0872","type":"print"},{"value":"1465-2080","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,12,1]]}}}