{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,12]],"date-time":"2026-09-12T06:33:49Z","timestamp":1789194829757,"version":"build-2803163510"},"reference-count":171,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,9,13]],"date-time":"2023-09-13T00:00:00Z","timestamp":1694563200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:p><jats:italic>Streptococcus pneumoniae<\/jats:italic> is a gram-positive, aerotolerant bacterium that naturally colonizes the human nasopharynx, but also causes invasive infections and is a major cause of morbidity and mortality worldwide. This pathogen produces high levels of H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> to eliminate other microorganisms that belong to the microbiota of the respiratory tract. However, it also induces an oxidative stress response to survive under this stressful condition. Furthermore, this self-defense mechanism is advantageous in tolerating oxidative stress imposed by the host\u2019s immune response. This review provides a comprehensive overview of the strategies employed by the pneumococcus to survive oxidative stress. These strategies encompass the utilization of H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> scavengers and thioredoxins, the adaptive response to antimicrobial host oxidants, the regulation of manganese and iron homeostasis, and the intricate regulatory networks that control the stress response. Here, we have also summarized less explored aspects such as the involvement of reparation systems and polyamine metabolism. A particular emphasis is put on the role of the oxidative stress response during the transient intracellular life of <jats:italic>Streptococcus pneumoniae<\/jats:italic>, including coinfection with influenza A and the induction of antibiotic persistence in host cells.<\/jats:p>","DOI":"10.3389\/fmicb.2023.1269843","type":"journal-article","created":{"date-parts":[[2023,9,13]],"date-time":"2023-09-13T21:46:10Z","timestamp":1694641570000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":29,"title":["The oxidative stress response of Streptococcus pneumoniae: its contribution to both extracellular and intracellular survival"],"prefix":"10.3389","volume":"14","author":[{"given":"Mirelys","family":"Hernandez-Morfa","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadia B.","family":"Olivero","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victoria E.","family":"Zappia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"German E.","family":"Pi\u00f1as","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicolas M.","family":"Reinoso-Vizcaino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melina B.","family":"Cian","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariana","family":"Nu\u00f1ez-Fernandez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paulo R.","family":"Cortes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jose","family":"Echenique","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,9,13]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"35615","DOI":"10.1074\/jbc.M110.172999","article-title":"Polymeric immunoglobulin receptor-mediated invasion of Streptococcus pneumoniae into host cells requires a coordinate signaling of SRC family of protein-tyrosine kinases, ERK, and c-Jun N-terminal kinase","volume":"285","author":"Agarwal","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref2","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1111\/cmi.12343","article-title":"Influenza virus replication in lung epithelial cells depends on redox-sensitive pathways activated by NOX4-derived ROS","volume":"17","author":"Amatore","year":"2015","journal-title":"Cell. Microbiol."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1128\/IAI.05563-11","article-title":"Pneumococcal gene complex involved in resistance to extracellular oxidative stress","volume":"80","author":"Andisi","year":"2012","journal-title":"Infect. Immun."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"e0043921","DOI":"10.1128\/JB.00439-21","article-title":"Pyruvate oxidase as a key determinant of pneumococcal viability during transcytosis across brain endothelium","volume":"203","author":"Anil","year":"2021","journal-title":"J. Bacteriol."},{"key":"ref5","doi-asserted-by":"publisher","first-page":"690","DOI":"10.1016\/j.bbrc.2010.07.002","article-title":"The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions","volume":"398","author":"Arenas","year":"2010","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref6","doi-asserted-by":"publisher","first-page":"890","DOI":"10.3390\/antiox11050890","article-title":"Halogenation activity of mammalian Heme peroxidases","volume":"11","author":"Arnhold","year":"2022","journal-title":"Antioxidants (Basel)"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"3691","DOI":"10.1099\/mic.0.031310-0","article-title":"Influence of a model human defensive peroxidase system on oral streptococcal antagonism","volume":"155","author":"Ashby","year":"2009","journal-title":"Microbiology (Reading)"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"1233","DOI":"10.1016\/j.ijmm.2014.10.001","article-title":"Endocytosis of Streptococcus pneumoniae via the polymeric immunoglobulin receptor of epithelial cells relies on clathrin and caveolin dependent mechanisms","volume":"304","author":"Asmat","year":"2014","journal-title":"Int. J. Med. Microbiol."},{"key":"ref9","doi-asserted-by":"publisher","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":"ref10","doi-asserted-by":"publisher","first-page":"578533","DOI":"10.3389\/fmicb.2020.578533","article-title":"SP_0916 is an arginine decarboxylase that catalyzes the synthesis of Agmatine, which is critical for capsule biosynthesis in Streptococcus pneumoniae","volume":"11","author":"Ayoola","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1996","DOI":"10.3389\/fmicb.2019.01996","article-title":"Polyamine synthesis effects capsule expression by reduction of precursors in Streptococcus pneumoniae","volume":"10","author":"Ayoola","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref12","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1038\/s41579-019-0196-3","article-title":"Definitions and guidelines for research on antibiotic persistence","volume":"17","author":"Balaban","year":"2019","journal-title":"Nat. Rev. Microbiol."},{"key":"ref13","doi-asserted-by":"publisher","first-page":"371465","DOI":"10.1155\/2013\/371465","article-title":"Role of oxidative stress in the pathophysiology of pneumococcal meningitis","volume":"2013","author":"Barichello","year":"2013","journal-title":"Oxidative Med. Cell. Longev."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1021\/tx200219s","article-title":"Hypothiocyanous acid: benign or deadly?","volume":"25","author":"Barrett","year":"2012","journal-title":"Chem. Res. Toxicol."},{"key":"ref15","doi-asserted-by":"publisher","first-page":"5255","DOI":"10.1128\/iai.64.12.5255-5262.1996","article-title":"Sequence heterogeneity of PsaA, a 37-kilodalton putative adhesin essential for virulence of Streptococcus pneumoniae","volume":"64","author":"Berry","year":"1996","journal-title":"Infect. Immun."},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1871","DOI":"10.1016\/S0140-6736(04)16357-5","article-title":"Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children","volume":"363","author":"Bogaert","year":"2004","journal-title":"Lancet"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"4123","DOI":"10.1099\/mic.0.028282-0","article-title":"The pneumococcal response to oxidative stress includes a role for Rgg","volume":"155","author":"Bortoni","year":"2009","journal-title":"Microbiology (Reading)"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"6357","DOI":"10.1128\/JB.00937-10","article-title":"Regulation of CodY activity through modulation of intracellular branched-chain amino acid pools","volume":"192","author":"Brinsmade","year":"2010","journal-title":"J. Bacteriol."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"e0251621","DOI":"10.1128\/mBio.02516-21","article-title":"Capsule promotes intracellular survival and vascular endothelial cell translocation during invasive pneumococcal disease","volume":"12","author":"Brissac","year":"2021","journal-title":"MBio"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1128\/IAI.00569-17","article-title":"Cell invasion and pyruvate oxidase-derived H(2)O(2) are critical for Streptococcus pneumoniae-mediated cardiomyocyte killing","volume":"86","author":"Brissac","year":"2018","journal-title":"Infect. Immun."},{"key":"ref21","doi-asserted-by":"publisher","first-page":"572","DOI":"10.1046\/j.1365-2958.2001.02414.x","article-title":"A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence","volume":"40","author":"Brown","year":"","journal-title":"Mol. Microbiol."},{"key":"ref22","doi-asserted-by":"publisher","first-page":"4389","DOI":"10.1128\/IAI.70.8.4389-4398.2002","article-title":"Characterization of pit, a Streptococcus pneumoniae iron uptake ABC transporter","volume":"70","author":"Brown","year":"2002","journal-title":"Infect. Immun."},{"key":"ref23","doi-asserted-by":"publisher","first-page":"6702","DOI":"10.1128\/IAI.69.11.6702-6706.2001","article-title":"Immunization with components of two iron uptake ABC transporters protects mice against systemic Streptococcus pneumoniae infection","volume":"69","author":"Brown","year":"","journal-title":"Infect. Immun."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"e68277","DOI":"10.1371\/journal.pone.0068277","article-title":"Pyruvate oxidase influences the sugar utilization pattern and capsule production in Streptococcus pneumoniae","volume":"8","author":"Carvalho","year":"2013","journal-title":"PLoS One"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"344","DOI":"10.1111\/j.1365-2958.2010.07339.x","article-title":"The global nutritional regulator CodY is an essential protein in the human pathogen Streptococcus pneumoniae","volume":"78","author":"Caymaris","year":"2010","journal-title":"Mol. Microbiol."},{"key":"ref26","year":"2012"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"e41393","DOI":"10.1371\/journal.pone.0041393","article-title":"Effects of deletion of the Streptococcus pneumoniae lipoprotein diacylglyceryl transferase gene lgt on ABC transporter function and on growth in vivo","volume":"7","author":"Chimalapati","year":"2012","journal-title":"PLoS One"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"807","DOI":"10.1111\/j.1348-0421.1999.tb02474.x","article-title":"Limited stress response in Streptococcus pneumoniae","volume":"43","author":"Choi","year":"1999","journal-title":"Microbiol. Immunol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1146\/annurev.micro.60.080805.142139","article-title":"Induction of competence regulons as a general response to stress in gram-positive bacteria","volume":"60","author":"Claverys","year":"2006","journal-title":"Annu. Rev. Microbiol."},{"key":"ref30","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1089\/ars.2010.3114","article-title":"Structure, function, and mechanism of thioredoxin proteins","volume":"13","author":"Collet","year":"2010","journal-title":"Antioxid. Redox Signal."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.ijmm.2014.12.002","article-title":"Stress-triggered signaling affecting survival or suicide of Streptococcus pneumoniae","volume":"305","author":"Cortes","year":"2015","journal-title":"Int. J. Med. Microbiol."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1038\/nchembio.1382","article-title":"Imperfect coordination chemistry facilitates metal ion release in the Psa permease","volume":"10","author":"Counago","year":"2014","journal-title":"Nat. Chem. Biol."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"12139","DOI":"10.3892\/mmr.2021.12139","article-title":"Oral peroxidases: from antimicrobial agents to ecological actors (review)","volume":"24","author":"Courtois","year":"2021","journal-title":"Mol. Med. Rep."},{"key":"ref34","doi-asserted-by":"publisher","first-page":"976273","DOI":"10.1155\/2012\/976273","article-title":"Global fluoroquinolone resistance epidemiology and implictions for clinical use","volume":"2012","author":"Dalhoff","year":"2012","journal-title":"Interdiscip. Perspect. Infect. Dis."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"3841","DOI":"10.1073\/pnas.1220341110","article-title":"Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens","volume":"110","author":"Damo","year":"2013","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref36","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1016\/j.bcp.2019.03.013","article-title":"The science of licking your wounds: function of oxidants in the innate immune system","volume":"163","author":"Day","year":"2019","journal-title":"Biochem. Pharmacol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"5701","DOI":"10.1007\/s00253-021-11360-5","article-title":"Relevance of peroxiredoxins in pathogenic microorganisms","volume":"105","author":"de Oliveira","year":"2021","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.1042\/bst0311322","article-title":"Prokaryotic Cu, Zn superoxide dismutases","volume":"31","author":"Desideri","year":"2003","journal-title":"Biochem. Soc. Trans."},{"key":"ref39","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1046\/j.1365-2958.1997.5111879.x","article-title":"Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases","volume":"25","author":"Dintilhac","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref40","doi-asserted-by":"publisher","first-page":"4392","DOI":"10.1128\/iai.61.10.4392-4397.1993","article-title":"Identification of hydrogen peroxide as a Streptococcus pneumoniae toxin for rat alveolar epithelial cells","volume":"61","author":"Duane","year":"1993","journal-title":"Infect. Immun."},{"key":"ref41","doi-asserted-by":"publisher","first-page":"2434","DOI":"10.1128\/IAI.72.4.2434-2437.2004","article-title":"Protein serine\/threonine kinase StkP positively controls virulence and competence in Streptococcus pneumoniae","volume":"72","author":"Echenique","year":"2004","journal-title":"Infect. Immun."},{"key":"ref42","doi-asserted-by":"publisher","first-page":"768","DOI":"10.1128\/JB.183.2.768-772.2001","article-title":"Competence modulation by the NADH oxidase of Streptococcus pneumoniae involves signal transduction","volume":"183","author":"Echenique","year":"2001","journal-title":"J. Bacteriol."},{"key":"ref44","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1111\/mmi.14557","article-title":"Role of the pyruvate metabolic network on carbohydrate metabolism and virulence in Streptococcus pneumoniae","volume":"114","author":"Echlin","year":"2020","journal-title":"Mol. Microbiol."},{"key":"ref43","doi-asserted-by":"publisher","first-page":"e1005951","DOI":"10.1371\/journal.ppat.1005951","article-title":"Pyruvate oxidase as a critical link between metabolism and capsule biosynthesis in Streptococcus pneumoniae","volume":"12","author":"Echlin","year":"2016","journal-title":"PLoS Pathog."},{"key":"ref45","doi-asserted-by":"publisher","first-page":"e89427","DOI":"10.1371\/journal.pone.0089427","article-title":"Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae","volume":"9","author":"Eijkelkamp","year":"2014","journal-title":"PLoS One"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"600","DOI":"10.1038\/s41564-018-0147-1","article-title":"Intracellular replication of Streptococcus pneumoniae inside splenic macrophages serves as a reservoir for septicaemia","volume":"3","author":"Ercoli","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref47","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1016\/j.bbapap.2004.08.017","article-title":"Methionine sulfoxide reductases in prokaryotes","volume":"1703","author":"Ezraty","year":"2005","journal-title":"Biochim. Biophys. Acta"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1097\/MCP.0000000000000674","article-title":"Pneumococcal virulence factors in community-acquired pneumonia","volume":"26","author":"Feldman","year":"2020","journal-title":"Curr. Opin. Pulm. Med."},{"key":"ref49","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1128\/AAC.02299-15","article-title":"Reactive oxygen species contribute to the bactericidal effects of the fluoroquinolone moxifloxacin in Streptococcus pneumoniae","volume":"60","author":"Ferrandiz","year":"2016","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref50","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1111\/mmi.14999","article-title":"The MerR-family regulator NmlR is involved in the defense against oxidative stress in Streptococcus pneumoniae","volume":"119","author":"Fritsch","year":"2023","journal-title":"Mol. Microbiol."},{"key":"ref51","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.chom.2009.09.005","article-title":"Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes","volume":"6","author":"Gannage","year":"2009","journal-title":"Cell Host Microbe"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1099\/00221287-144-2-433","article-title":"Organization around the dnaA gene of Streptococcus pneumoniae","volume":"144","author":"Gasc","year":"1998","journal-title":"Microbiology (Reading)"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"e0270122","DOI":"10.1128\/spectrum.02701-22","article-title":"Antibiotic tolerance indicative of persistence is pervasive among clinical Streptococcus pneumoniae isolates and shows strong condition dependence","volume":"10","author":"Geerts","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref54","doi-asserted-by":"publisher","first-page":"1798","DOI":"10.1002\/emmm.201303482","article-title":"The 'captain of the men of death', Streptococcus pneumoniae, fights oxidative stress outside the 'city wall'","volume":"5","author":"Gennaris","year":"2013","journal-title":"EMBO Mol. Med."},{"key":"ref9001","first-page":"1","article-title":"Pneumococcal disease","volume-title":"Epidemiology and Prevention of Vaccine-Preventable Diseases -14th edition","author":"Gierke","year":"2021"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"e0236389","DOI":"10.1371\/journal.pone.0236389","article-title":"Oxidative killing of encapsulated and nonencapsulated Streptococcus pneumoniae by lactoperoxidase-generated hypothiocyanite","volume":"15","author":"Gingerich","year":"2020","journal-title":"PLoS One"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"e1007052","DOI":"10.1371\/journal.ppat.1007052","article-title":"RitR is an archetype for a novel family of redox sensors in the streptococci that has evolved from two-component response regulators and is required for pneumococcal colonization","volume":"14","author":"Glanville","year":"2018","journal-title":"PLoS Pathog."},{"key":"ref57","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1016\/j.ijmm.2017.11.012","article-title":"Streptococcus pneumoniae two-component regulatory systems: the interplay of the pneumococcus with its environment","volume":"308","author":"Gomez-Mejia","year":"2018","journal-title":"Int. J. Med. Microbiol."},{"key":"ref58","doi-asserted-by":"publisher","first-page":"e65626","DOI":"10.1371\/journal.pone.0065626","article-title":"Streptococcus pneumoniae invades endothelial host cells via multiple pathways and is killed in a lysosome dependent manner","volume":"8","author":"Gradstedt","year":"2013","journal-title":"PLoS One"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"4333","DOI":"10.1128\/IAI.00126-12","article-title":"Thiol peroxidase is an important component of Streptococcus pneumoniae in oxygenated environments","volume":"80","author":"Hajaj","year":"2012","journal-title":"Infect. Immun."},{"key":"ref60","doi-asserted-by":"publisher","first-page":"210","DOI":"10.3389\/fcimb.2017.00210","article-title":"CodY regulates thiol peroxidase expression as part of the pneumococcal defense mechanism against H(2)O(2) stress","volume":"7","author":"Hajaj","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref61","doi-asserted-by":"publisher","first-page":"1487","DOI":"10.1128\/mBio.01487-17","article-title":"The NOX Family of proteins is also present in Bacteria","volume":"8","author":"Hajjar","year":"2017","journal-title":"MBio"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1111\/j.1365-2958.2007.05900.x","article-title":"Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs","volume":"66","author":"Halfmann","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref63","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.semcdb.2020.12.005","article-title":"Iron in immune cell function and host defense","volume":"115","author":"Haschka","year":"2021","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref64","doi-asserted-by":"publisher","first-page":"1389","DOI":"10.1046\/j.1365-2958.2002.03106.x","article-title":"Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors","volume":"45","author":"Hava","year":"2002","journal-title":"Mol. Microbiol."},{"key":"ref65","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1128\/JB.00917-07","article-title":"CodY of Streptococcus pneumoniae: link between nutritional gene regulation and colonization","volume":"190","author":"Hendriksen","year":"2008","journal-title":"J. Bacteriol."},{"key":"ref66","doi-asserted-by":"publisher","first-page":"1569","DOI":"10.1099\/mic.0.025072-0","article-title":"Strain-specific impact of PsaR of Streptococcus pneumoniae on global gene expression and virulence","volume":"155","author":"Hendriksen","year":"2009","journal-title":"Microbiology (Reading)"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"e0436422","DOI":"10.1128\/spectrum.04364-22","article-title":"Host cell oxidative stress promotes intracellular fluoroquinolone Persisters of Streptococcus pneumoniae","volume":"10","author":"Hernandez-Morfa","year":"2022","journal-title":"Microbiol. Spectr."},{"key":"ref68","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1111\/j.1399-302X.1992.tb00594.x","article-title":"Reduced nicotinamide adenine dinucleotide oxidase involvement in defense against oxygen toxicity of Streptococcus mutans","volume":"7","author":"Higuchi","year":"1992","journal-title":"Oral Microbiol. Immunol."},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1365","DOI":"10.3390\/microorganisms9071365","article-title":"The two-component system 09 of Streptococcus pneumoniae is important for metabolic fitness and resistance during dissemination in the host","volume":"9","author":"Hirschmann","year":"2021","journal-title":"Microorganisms"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1111\/j.1751-7915.2011.00327.x","article-title":"Bacterial persistence increases as environmental fitness decreases","volume":"5","author":"Hong","year":"2012","journal-title":"Microb. Biotechnol."},{"key":"ref71","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1038\/nrmicro2836","article-title":"Nutritional immunity: transition metals at the pathogen-host interface","volume":"10","author":"Hood","year":"2012","journal-title":"Nat. Rev. Microbiol."},{"key":"ref72","doi-asserted-by":"publisher","first-page":"3939","DOI":"10.1128\/IAI.01829-14","article-title":"Effect of nonheme iron-containing ferritin Dpr in the stress response and virulence of pneumococci","volume":"82","author":"Hua","year":"2014","journal-title":"Infect. Immun."},{"key":"ref73","doi-asserted-by":"publisher","first-page":"5258","DOI":"10.1128\/JB.186.16.5258-5266.2004","article-title":"Control of virulence by the two-component system CiaR\/H is mediated via HtrA, a major virulence factor of Streptococcus pneumoniae","volume":"186","author":"Ibrahim","year":"2004","journal-title":"J. Bacteriol."},{"key":"ref74","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1039\/C0MT00050G","article-title":"Interplay between manganese and zinc homeostasis in the human pathogen Streptococcus pneumoniae","volume":"3","author":"Jacobsen","year":"2011","journal-title":"Metallomics"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"1709","DOI":"10.1099\/00221287-147-7-1709","article-title":"Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria","volume":"147","author":"Jakubovics","year":"2001","journal-title":"Microbiology (Reading)"},{"key":"ref76","doi-asserted-by":"publisher","first-page":"6829","DOI":"10.3892\/ol.2019.10997","article-title":"Sufentanil impairs autophagic degradation and inhibits cell migration in NCI-H460 in vitro","volume":"18","author":"Jiang","year":"2019","journal-title":"Oncol. Lett."},{"key":"ref77","doi-asserted-by":"publisher","first-page":"e0123702","DOI":"10.1371\/journal.pone.0123702","article-title":"Co-inactivation of GlnR and CodY regulators impacts pneumococcal Cell Wall physiology","volume":"10","author":"Johnston","year":"2015","journal-title":"PLoS One"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1128\/IAI.74.2.1171-1180.2006","article-title":"Mn2+\u2212dependent regulation of multiple genes in Streptococcus pneumoniae through PsaR and the resultant impact on virulence","volume":"74","author":"Johnston","year":"2006","journal-title":"Infect. Immun."},{"key":"ref79","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1016\/j.sbi.2020.09.012","article-title":"Structural determinants of regulated proteolysis in pathogenic bacteria by ClpP and the proteasome","volume":"67","author":"Kahne","year":"2021","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref80","doi-asserted-by":"publisher","first-page":"2013","DOI":"10.1128\/microbiolspec.MGM2-0002-2013","article-title":"Genetics of mycobacterial Trehalose metabolism","volume":"2","author":"Kalscheuer","year":"2014","journal-title":"Microbiol. Spectr."},{"key":"ref82","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1086\/514205","article-title":"Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae","volume":"177","author":"Kim","year":"1998","journal-title":"J. Infect. Dis."},{"key":"ref81","doi-asserted-by":"publisher","first-page":"699","DOI":"10.1111\/j.1365-2958.2009.06680.x","article-title":"Structural and kinetic analysis of an MsrA-MsrB fusion protein from Streptococcus pneumoniae","volume":"72","author":"Kim","year":"2009","journal-title":"Mol. Microbiol."},{"key":"ref83","doi-asserted-by":"publisher","first-page":"25097","DOI":"10.1074\/jbc.M601661200","article-title":"Regulation of glutamine and glutamate metabolism by GlnR and GlnA in Streptococcus pneumoniae","volume":"281","author":"Kloosterman","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref84","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1086\/367935","article-title":"The role of clonality in the global spread of fluoroquinolone-resistant bacteria","volume":"36","author":"Klugman","year":"2003","journal-title":"Clin. Infect. Dis."},{"key":"ref85","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.mib.2018.10.004","article-title":"Modulation of bacterial virulence and fitness by host glutathione","volume":"47","author":"Ku","year":"2019","journal-title":"Curr. Opin. Microbiol."},{"key":"ref86","doi-asserted-by":"publisher","first-page":"3757","DOI":"10.1128\/IAI.71.7.3757-3765.2003","article-title":"Effect of heat shock and mutations in ClpL and ClpP on virulence gene expression in Streptococcus pneumoniae","volume":"71","author":"Kwon","year":"2003","journal-title":"Infect. Immun."},{"key":"ref87","doi-asserted-by":"publisher","first-page":"5035","DOI":"10.1128\/iai.64.12.5035-5041.1996","article-title":"Cloning and molecular characterization of cu,Zn superoxide dismutase from Actinobacillus pleuropneumoniae","volume":"64","author":"Langford","year":"1996","journal-title":"Infect. Immun."},{"key":"ref89","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1111\/j.1365-2249.2004.02628.x","article-title":"Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse","volume":"138","author":"Ling","year":"2004","journal-title":"Clin. Exp. Immunol."},{"key":"ref88","doi-asserted-by":"publisher","first-page":"e0122753","DOI":"10.1371\/journal.pone.0122753","article-title":"Streptococcus pneumoniae induces autophagy through the inhibition of the PI3K-I\/Akt\/mTOR pathway and ROS hypergeneration in A549 cells","volume":"10","author":"Li","year":"2015","journal-title":"PLoS One"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"7689","DOI":"10.1021\/bi401132w","article-title":"Physical characterization of the manganese-sensing pneumococcal surface antigen repressor from Streptococcus pneumoniae","volume":"52","author":"Lisher","year":"2013","journal-title":"Biochemistry"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1128\/mSphere.00291-16","article-title":"Biological and chemical adaptation to endogenous hydrogen peroxide production in Streptococcus pneumoniae D39","volume":"2","author":"Lisher","year":"2017","journal-title":"mSphere"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"580","DOI":"10.1016\/j.micinf.2017.08.008","article-title":"The role of oxidative stress in influenza virus infection","volume":"19","author":"Liu","year":"2017","journal-title":"Microbes Infect."},{"key":"ref93","doi-asserted-by":"publisher","first-page":"26480","DOI":"10.1074\/jbc.R113.467738","article-title":"The redox biochemistry of protein sulfenylation and sulfinylation","volume":"288","author":"Lo Conte","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref94","doi-asserted-by":"publisher","first-page":"e0141816","DOI":"10.1371\/journal.pone.0141816","article-title":"Characterization of pneumococcal genes involved in bloodstream invasion in a mouse model","volume":"10","author":"Mahdi","year":"2015","journal-title":"PLoS One"},{"key":"ref95","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1146\/annurev-biochem-062917-012848","article-title":"Regulated proteolysis in Bacteria","volume":"87","author":"Mahmoud","year":"2018","journal-title":"Annu. Rev. Biochem."},{"key":"ref96","doi-asserted-by":"publisher","first-page":"D200","DOI":"10.1093\/nar\/gkw1129","article-title":"CDD\/SPARCLE: functional classification of proteins via subfamily domain architectures","volume":"45","author":"Marchler-Bauer","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref97","doi-asserted-by":"publisher","first-page":"2145","DOI":"10.1016\/j.biochi.2013.08.008","article-title":"The thioredoxin system in the dental caries pathogen Streptococcus mutans and the food-industry bacterium Streptococcus thermophilus","volume":"95","author":"Marco","year":"2013","journal-title":"Biochimie"},{"key":"ref98","doi-asserted-by":"publisher","first-page":"1483","DOI":"10.1099\/00221287-148-5-1483","article-title":"In vivo characterization of the psa genes from Streptococcus pneumoniae in multiple models of infection","volume":"148","author":"Marra","year":"2002","journal-title":"Microbiology (Reading)"},{"key":"ref99","doi-asserted-by":"publisher","first-page":"6885","DOI":"10.1093\/nar\/gkz494","article-title":"A Mn-sensing riboswitch activates expression of a Mn2+\/Ca2+ ATPase transporter in Streptococcus","volume":"47","author":"Martin","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref100","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1128\/JB.185.1.60-70.2003","article-title":"The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis","volume":"185","author":"Mascher","year":"2003","journal-title":"J. Bacteriol."},{"key":"ref101","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1111\/j.1365-2958.2004.04164.x","article-title":"Molecular analysis of the psa permease complex of Streptococcus pneumoniae","volume":"53","author":"McAllister","year":"2004","journal-title":"Mol. Microbiol."},{"key":"ref102","doi-asserted-by":"publisher","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":"ref103","doi-asserted-by":"publisher","first-page":"5753","DOI":"10.1016\/S0021-9258(18)91929-0","article-title":"The reduction of cytochrome c by milk xanthine oxidase","volume":"243","author":"McCord","year":"1968","journal-title":"J. Biol. Chem."},{"key":"ref104","doi-asserted-by":"publisher","first-page":"e1002357","DOI":"10.1371\/journal.ppat.1002357","article-title":"A molecular mechanism for bacterial susceptibility to zinc","volume":"7","author":"McDevitt","year":"2011","journal-title":"PLoS Pathog."},{"key":"ref105","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.drup.2016.10.002","article-title":"Molecular mechanisms and clinical implications of bacterial persistence","volume":"29","author":"Michiels","year":"2016","journal-title":"Drug Resist. Updat."},{"key":"ref106","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1016\/j.abb.2012.04.014","article-title":"Why do bacteria use so many enzymes to scavenge hydrogen peroxide?","volume":"525","author":"Mishra","year":"2012","journal-title":"Arch. Biochem. Biophys."},{"key":"ref107","doi-asserted-by":"publisher","first-page":"314","DOI":"10.1038\/s41598-017-18645-8","article-title":"Flavin reductase contributes to pneumococcal virulence by protecting from oxidative stress and mediating adhesion and elicits protection against pneumococcal challenge","volume":"8","author":"Morozov","year":"2018","journal-title":"Sci. Rep."},{"key":"ref108","doi-asserted-by":"publisher","first-page":"10008","DOI":"10.3390\/medsci6010008","article-title":"The role of Cadaverine synthesis on pneumococcal capsule and protein expression","volume":"6","author":"Nakamya","year":"2018","journal-title":"Med Sci (Basel)"},{"key":"ref109","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.3390\/pathogens10101322","article-title":"The effect of impaired polyamine transport on pneumococcal transcriptome","volume":"10","author":"Nakamya","year":"2021","journal-title":"Pathogens"},{"key":"ref110","doi-asserted-by":"publisher","first-page":"982","DOI":"10.1126\/science.1211037","article-title":"Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria","volume":"334","author":"Nguyen","year":"2011","journal-title":"Science"},{"key":"ref9002","doi-asserted-by":"publisher","first-page":"1243","DOI":"10.1111\/j.1742-4658.2005.04560.x","article-title":"Characterization of a eukaryotic type serine\/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates","volume":"72","author":"Nov\u00e1kov\u00e1","year":"2005","journal-title":"FEBS J."},{"key":"ref111","doi-asserted-by":"publisher","first-page":"1285","DOI":"10.1046\/j.1365-2958.1998.01016.x","article-title":"Penicillin tolerance genes of Streptococcus pneumoniae: the ABC-type manganese permease complex Psa","volume":"29","author":"Novak","year":"1998","journal-title":"Mol. Microbiol."},{"key":"ref112","doi-asserted-by":"publisher","first-page":"e12846","DOI":"10.1111\/cmi.12846","article-title":"Molecular mechanisms of Streptococcus pneumoniae-targeted autophagy via pneumolysin, Golgi-resident Rab41, and Nedd4-1-mediated K63-linked ubiquitination","volume":"20","author":"Ogawa","year":"2018","journal-title":"Cell. Microbiol."},{"key":"ref113","doi-asserted-by":"publisher","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":"ref114","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1128\/IAI.00805-12","article-title":"Interplay between manganese and iron in pneumococcal pathogenesis: role of the orphan response regulator RitR","volume":"81","author":"Ong","year":"2013","journal-title":"Infect. Immun."},{"key":"ref115","doi-asserted-by":"publisher","first-page":"e1011493","DOI":"10.1371\/journal.ppat.1011493","article-title":"S100A9 is indispensable for survival of pneumococcal pneumonia in mice","volume":"19","author":"Ostermann","year":"2023","journal-title":"PLoS Pathog."},{"key":"ref116","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/s12275-010-9300-0","article-title":"Virulence attenuation of Streptococcus pneumoniae clpP mutant by sensitivity to oxidative stress in macrophages via an NO-mediated pathway","volume":"48","author":"Park","year":"2010","journal-title":"J. Microbiol."},{"key":"ref117","doi-asserted-by":"publisher","first-page":"1352","DOI":"10.1111\/febs.13228","article-title":"ClpL is a chaperone without auxiliary factors","volume":"282","author":"Park","year":"2015","journal-title":"FEBS J."},{"key":"ref118","doi-asserted-by":"publisher","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":"ref119","doi-asserted-by":"publisher","first-page":"4583","DOI":"10.1074\/jbc.M117.775213","article-title":"Pre-steady-state kinetics reveal the substrate specificity and mechanism of halide oxidation of truncated human Peroxidasin 1","volume":"292","author":"Paumann-Page","year":"2017","journal-title":"J. Biol. Chem."},{"key":"ref120","doi-asserted-by":"publisher","first-page":"3990","DOI":"10.1128\/IAI.68.7.3990-3997.2000","article-title":"Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract","volume":"68","author":"Pericone","year":"2000","journal-title":"Infect. Immun."},{"key":"ref121","doi-asserted-by":"publisher","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":"ref122","doi-asserted-by":"publisher","first-page":"1300","DOI":"10.1099\/mic.0.2007\/015925-0","article-title":"Acidic stress induces autolysis by a CSP-independent ComE pathway in Streptococcus pneumoniae","volume":"154","author":"Pinas","year":"2008","journal-title":"Microbiology (Reading)"},{"key":"ref123","doi-asserted-by":"publisher","first-page":"e1007118","DOI":"10.1371\/journal.ppat.1007118","article-title":"Crosstalk between the serine\/threonine kinase StkP and the response regulator ComE controls the stress response and intracellular survival of Streptococcus pneumoniae","volume":"14","author":"Pinas","year":"2018","journal-title":"PLoS Pathog."},{"key":"ref124","doi-asserted-by":"publisher","first-page":"4063","DOI":"10.1128\/JB.00383-10","article-title":"The MerR\/NmlR family transcription factor of Streptococcus pneumoniae responds to carbonyl stress and modulates hydrogen peroxide production","volume":"192","author":"Potter","year":"2010","journal-title":"J. Bacteriol."},{"key":"ref125","doi-asserted-by":"publisher","first-page":"6248","DOI":"10.1128\/JB.01393-12","article-title":"Streptococcus pneumoniae uses glutathione to defend against oxidative stress and metal ion toxicity","volume":"194","author":"Potter","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref126","doi-asserted-by":"publisher","first-page":"7827","DOI":"10.1128\/IAI.73.12.7827-7835.2005","article-title":"beta-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae","volume":"73","author":"Radin","year":"2005","journal-title":"Infect. Immun."},{"key":"ref127","doi-asserted-by":"publisher","first-page":"E3421","DOI":"10.1073\/pnas.1424144112","article-title":"Streptococcus pneumoniae secretes hydrogen peroxide leading to DNA damage and apoptosis in lung cells","volume":"112","author":"Rai","year":"2015","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref128","doi-asserted-by":"publisher","first-page":"9095275","DOI":"10.1155\/2018\/9095275","article-title":"Eosinophils from physiology to disease: a comprehensive review","volume":"2018","author":"Ramirez","year":"2018","journal-title":"Biomed. Res. Int."},{"key":"ref129","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1111\/j.1365-2958.2007.06082.x","article-title":"Polymorphism and regulation of the spxB (pyruvate oxidase) virulence factor gene by a CBS-HotDog domain protein (SpxR) in serotype 2 Streptococcus pneumoniae","volume":"67","author":"Ramos-Montanez","year":"2008","journal-title":"Mol. Microbiol."},{"key":"ref130","doi-asserted-by":"publisher","first-page":"3366","DOI":"10.4049\/jimmunol.180.5.3366","article-title":"Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia","volume":"180","author":"Raquil","year":"2008","journal-title":"J. Immunol."},{"key":"ref131","doi-asserted-by":"publisher","first-page":"6532","DOI":"10.1128\/JB.00813-07","article-title":"SpxB is a suicide gene of Streptococcus pneumoniae and confers a selective advantage in an in vivo competitive colonization model","volume":"189","author":"Regev-Yochay","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref132","doi-asserted-by":"publisher","first-page":"e1008761","DOI":"10.1371\/journal.ppat.1008761","article-title":"The pneumococcal two-component system SirRH is linked to enhanced intracellular survival of Streptococcus pneumoniae in influenza-infected pulmonary cells","volume":"16","author":"Reinoso-Vizcaino","year":"2020","journal-title":"PLoS Pathog."},{"key":"ref133","doi-asserted-by":"publisher","first-page":"953","DOI":"10.1093\/infdis\/jiw268","article-title":"Thioredoxins and methionine sulfoxide reductases in the pathophysiology of pneumococcal meningitis","volume":"214","author":"Ribes","year":"2016","journal-title":"J. Infect. Dis."},{"key":"ref134","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1172\/JCI2406","article-title":"Pneumococcal trafficking across the blood-brain barrier. Molecular analysis of a novel bidirectional pathway","volume":"102","author":"Ring","year":"1998","journal-title":"J. Clin. Invest."},{"key":"ref135","doi-asserted-by":"publisher","first-page":"3508","DOI":"10.1128\/JB.184.13.3508-3520.2002","article-title":"Global transcriptional analysis of clpP mutations of type 2 Streptococcus pneumoniae and their effects on physiology and virulence","volume":"184","author":"Robertson","year":"2002","journal-title":"J. Bacteriol."},{"key":"ref136","doi-asserted-by":"publisher","first-page":"12","DOI":"10.1111\/j.1365-2958.2009.06638.x","article-title":"Role of the manganese efflux system mntE for signalling and pathogenesis in Streptococcus pneumoniae","volume":"72","author":"Rosch","year":"2009","journal-title":"Mol. Microbiol."},{"key":"ref137","doi-asserted-by":"publisher","first-page":"mfac001","DOI":"10.1093\/mtomcs\/mfac001","article-title":"Zinc sequestration by human calprotectin facilitates manganese binding to the bacterial solute-binding proteins PsaA and MntC","volume":"14","author":"Rosen","year":"2022","journal-title":"Metallomics"},{"key":"ref138","doi-asserted-by":"publisher","first-page":"111862","DOI":"10.1016\/j.jinorgbio.2022.111862","article-title":"S100A12 promotes Mn(II) binding to pneumococcal PsaA and staphylococcal MntC by Zn(II) sequestration","volume":"233","author":"Rosen","year":"2022","journal-title":"J. Inorg. Biochem."},{"key":"ref139","doi-asserted-by":"publisher","first-page":"1459","DOI":"10.1126\/science.1318579","article-title":"Cytochrome b558: the flavin-binding component of the phagocyte NADPH oxidase","volume":"256","author":"Rotrosen","year":"1992","journal-title":"Science"},{"key":"ref141","doi-asserted-by":"publisher","first-page":"1852","DOI":"10.1002\/emmm.201202435","article-title":"Molecular architecture of Streptococcus pneumoniae surface thioredoxin-fold lipoproteins crucial for extracellular oxidative stress resistance and maintenance of virulence","volume":"5","author":"Saleh","year":"2013","journal-title":"EMBO Mol. Med."},{"key":"ref9003","doi-asserted-by":"publisher","first-page":"4168","DOI":"10.1128\/JB.01616-06","article-title":"Eukaryotic-type serine\/threonine protein kinase StkP is a global regulator of gene expression in Streptococcus pneumoniae","volume":"189","author":"Saskov\u00e1","year":"2007","journal-title":"J. Bacteriol."},{"key":"ref142","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/0304-4165(85)90115-1","article-title":"Binding of manganese in human and rat plasma","volume":"840","author":"Scheuhammer","year":"1985","journal-title":"Biochim. Biophys. Acta"},{"key":"ref143","doi-asserted-by":"publisher","first-page":"7173","DOI":"10.1128\/JB.183.24.7173-7181.2001","article-title":"Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli","volume":"183","author":"Seaver","year":"2001","journal-title":"J. Bacteriol."},{"key":"ref144","doi-asserted-by":"publisher","first-page":"4059","DOI":"10.1128\/IAI.70.8.4059-4067.2002","article-title":"Microarray-based identification of htrA, a Streptococcus pneumoniae gene that is regulated by the CiaRH two-component system and contributes to nasopharyngeal colonization","volume":"70","author":"Sebert","year":"2002","journal-title":"Infect. Immun."},{"key":"ref145","doi-asserted-by":"publisher","first-page":"643326","DOI":"10.3389\/fcimb.2021.643326","article-title":"Virus-induced changes of the respiratory tract environment promote secondary infections with Streptococcus pneumoniae","volume":"11","author":"Sender","year":"2021","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref146","doi-asserted-by":"publisher","first-page":"31386","DOI":"10.1073\/pnas.2012265117","article-title":"Capillary leakage provides nutrients and antioxidants for rapid pneumococcal proliferation in influenza-infected lower airways","volume":"117","author":"Sender","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref147","doi-asserted-by":"publisher","first-page":"504","DOI":"10.1099\/mic.0.042564-0","article-title":"Polyamine biosynthesis and transport mechanisms are crucial for fitness and pathogenesis of Streptococcus pneumoniae","volume":"157","author":"Shah","year":"2011","journal-title":"Microbiology (Reading)"},{"key":"ref148","doi-asserted-by":"publisher","first-page":"e0053021","DOI":"10.1128\/IAI.00530-21","article-title":"Resistance of Streptococcus pneumoniae to Hypothiocyanous acid generated by host peroxidases","volume":"90","author":"Shearer","year":"","journal-title":"Infect. Immun."},{"key":"ref149","doi-asserted-by":"publisher","first-page":"102359","DOI":"10.1016\/j.jbc.2022.102359","article-title":"A newly identified flavoprotein disulfide reductase Har protects Streptococcus pneumoniae against hypothiocyanous acid","volume":"298","author":"Shearer","year":"","journal-title":"J. Biol. Chem."},{"key":"ref150","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.freeradbiomed.2021.12.261","article-title":"Glutathione utilization protects Streptococcus pneumoniae against lactoperoxidase-derived hypothiocyanous acid","volume":"179","author":"Shearer","year":"","journal-title":"Free Radic. Biol. Med."},{"key":"ref151","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.coi.2019.04.002","article-title":"Metals as phagocyte antimicrobial effectors","volume":"60","author":"Sheldon","year":"2019","journal-title":"Curr. Opin. Immunol."},{"key":"ref152","doi-asserted-by":"publisher","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":"ref153","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1128\/jb.162.3.1255-1260.1985","article-title":"Bacteriocuprein superoxide dismutases in pseudomonads","volume":"162","author":"Steinman","year":"1985","journal-title":"J. Bacteriol."},{"key":"ref154","doi-asserted-by":"publisher","first-page":"927","DOI":"10.1111\/brv.12140","article-title":"The return of metabolism: biochemistry and physiology of the pentose phosphate pathway","volume":"90","author":"Stincone","year":"2015","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref155","doi-asserted-by":"crossref","first-page":"245","DOI":"10.33549\/physiolres.930448","article-title":"Calprotectin \u2013 a pleiotropic molecule in acute and chronic inflammation","volume":"53","author":"Striz","year":"2004","journal-title":"Physiol. Res."},{"key":"ref156","doi-asserted-by":"publisher","first-page":"e13077","DOI":"10.1111\/cmi.13077","article-title":"Emerging concepts in the pathogenesis of the Streptococcus pneumoniae: from nasopharyngeal colonizer to intracellular pathogen","volume":"21","author":"Subramanian","year":"2019","journal-title":"Cell. Microbiol."},{"key":"ref157","doi-asserted-by":"publisher","first-page":"3772","DOI":"10.1128\/iai.64.9.3772-3777.1996","article-title":"Uptake of Streptococcus pneumoniae by respiratory epithelial cells","volume":"64","author":"Talbot","year":"1996","journal-title":"Infect. Immun."},{"key":"ref158","doi-asserted-by":"publisher","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":"ref159","doi-asserted-by":"publisher","first-page":"385","DOI":"10.1007\/s00018-020-03591-y","article-title":"The effects of neutrophil-generated hypochlorous acid and other hypohalous acids on host and pathogens","volume":"78","author":"Ulfig","year":"2021","journal-title":"Cell. Mol. Life Sci."},{"key":"ref160","doi-asserted-by":"publisher","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":"ref161","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1111\/j.1365-2958.2008.06532.x","article-title":"Phosphorylation of the RitR DNA-binding domain by a Ser-Thr phosphokinase: implications for global gene regulation in the streptococci","volume":"71","author":"Ulijasz","year":"2009","journal-title":"Mol. Microbiol."},{"key":"ref162","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1038\/nchembio.915","article-title":"Signaling-mediated bacterial persister formation","volume":"8","author":"Vega","year":"2012","journal-title":"Nat. Chem. Biol."},{"key":"ref163","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1080\/15548627.2019.1580089","article-title":"Influenza M2 protein regulates MAVS-mediated signaling pathway through interacting with MAVS and increasing ROS production","volume":"15","author":"Wang","year":"2019","journal-title":"Autophagy"},{"key":"ref164","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1146\/annurev-biochem-060815-014442","article-title":"Reactive oxygen species and neutrophil function","volume":"85","author":"Winterbourn","year":"2016","journal-title":"Annu. Rev. Biochem."},{"key":"ref166","doi-asserted-by":"publisher","first-page":"8569","DOI":"10.1073\/pnas.0308514101","article-title":"Crystal structure of nickel-containing superoxide dismutase reveals another type of active site","volume":"101","author":"Wuerges","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"ref165","doi-asserted-by":"publisher","first-page":"4922","DOI":"10.1128\/AAC.00921-12","article-title":"Role of oxidative stress in persister tolerance","volume":"56","author":"Wu","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref167","doi-asserted-by":"publisher","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":"ref168","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1099\/00221287-147-2-431","article-title":"Characterization of the Streptococcus pneumoniae NADH oxidase that is required for infection","volume":"147","author":"Yu","year":"2001","journal-title":"Microbiology (Reading)"},{"key":"ref169","doi-asserted-by":"publisher","first-page":"102046","DOI":"10.1016\/j.jbc.2022.102046","article-title":"SifR is an Rrf2-family quinone sensor associated with catechol iron uptake in Streptococcus pneumoniae D39","volume":"298","author":"Zhang","year":"2022","journal-title":"J. Biol. Chem."}],"container-title":["Frontiers in Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1269843\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,18]],"date-time":"2023-09-18T07:02:52Z","timestamp":1695020572000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmicb.2023.1269843\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,13]]},"references-count":171,"alternative-id":["10.3389\/fmicb.2023.1269843"],"URL":"https:\/\/doi.org\/10.3389\/fmicb.2023.1269843","relation":{},"ISSN":["1664-302X"],"issn-type":[{"value":"1664-302X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,13]]},"article-number":"1269843"}}