Disentangling competence for genetic transformation and virulence in Streptococcus pneumoniae

详细信息    查看全文

• 作者：Jingjun Lin ; Luchang Zhu ; Gee W. Lau
• 关键词：Streptococcus pneumoniae ; Competence ; Virulence ; Allolysis ; Pneumolysin
• 刊名：Current Genetics
• 出版年：2016
• 出版时间：February 2016
• 年：2016
• 卷：62
• 期：1
• 页码：97-103
• 全文大小：778 KB
• 参考文献：Alhamdi Y, Neill DR, Abrams ST, Malak HA, Yahya R, Barrett-Jolley R, Wang G, Kadioglu A, Toh CH (2015) Circulating pneumolysin is a potent inducer of cardiac injury during pneumococcal infection. PLoS Pathog 11:e1004836. doi:10.​1371/​journal.​ppat.​1004836 PubMedCentral CrossRef PubMed
  Benton KA, Everson MP, Briles DE (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63:448–455PubMedCentral PubMed
  Berry AM, Lock RA, Hansman D, Paton JC (1989a) Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect Immun 57:2324–2330PubMedCentral PubMed
  Berry AM, Yother J, Briles DE, Hansman D, Paton JC (1989b) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57:2037–2042PubMedCentral PubMed
  Brown AO, Mann B, Gao G, Hankins JS, Humann J, Giardina J, Faverio P, Restrepo MI, Halade GV, Mortensen EM, Lindsey ML, Hanes M, Happel KI, Nelson S, Bagby GJ, Lorent JA, Cardinal P, Granados R, Esteban A, LeSaux CJ, Tuomanen EI, Orihuela CJ (2014) Streptococcus pneumoniae translocates into the myocardium and forms unique microlesions that disrupt cardiac function. PLoS Pathog 10:e1004383. doi:10.​1371/​journal.​ppat.​1004383 PubMedCentral CrossRef PubMed
  Chancey ST, Agrawal S, Schroeder MR, Farley MM, Tettelin H, Stephens DS (2015) Composite mobile genetic elements disseminating macrolide resistance in Streptococcus pneumoniae. Front Microbiol 6:26. doi:10.​3389/​fmicb.​2015.​00026 PubMedCentral CrossRef PubMed
  Claverys JP, Prudhomme M, Martin B (2006) Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60:451–475. doi:10.​1146/​annurev.​micro.​60.​080805.​142139 CrossRef PubMed
  Claverys JP, Martin B, Havarstein LS (2007) Competence-induced fratricide in streptococci. Mol Microbiol 64:1423–1433. doi:10.​1111/​j.​1365-2958.​2007.​05757.​x CrossRef PubMed
  Copin R, Vitry MA, Hanot Mambres D, Machelart A, De Trez C, Vanderwinden JM, Magez S, Akira S, Ryffel B, Carlier Y, Letesson JJ, Muraille E (2012) In situ microscopy analysis reveals local innate immune response developed around Brucella infected cells in resistant and susceptible mice. PLoS Pathog 8:e1002575. doi:10.​1371/​journal.​ppat.​1002575 PubMedCentral CrossRef PubMed
  Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, Pichon B, Baker S, Parry CM, Lambertsen LM, Shahinas D, Pillai DR, Mitchell TJ, Dougan G, Tomasz A, Klugman KP, Parkhill J, Hanage WP, Bentley SD (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331:430–434. doi:10.​1126/​science.​1198545 PubMedCentral CrossRef PubMed
  Dai C, Basilico P, Cremona TP, Collins P, Moser B, Benarafa C, Wolf M (2015) CXCL14 displays antimicrobial activity against respiratory tract bacteria and contributes to clearance of Streptococcus pneumoniae pulmonary infection. J Immunol 194:5980–5989. doi:10.​4049/​jimmunol.​1402634 CrossRef PubMed
  Davis KM, Mohammadi S, Isberg RR (2015) Community behavior and spatial regulation within a bacterial microcolony in deep tissue sites serves to protect against host attack. Cell Host Microbe 17:21–31. doi:10.​1016/​j.​chom.​2014.​11.​008 PubMedCentral CrossRef PubMed
  Ebner P, Rinker J, Gotz F (2015) Excretion of cytoplasmic proteins in Staphylococcus is most likely not due to cell lysis. Curr Genet. doi:10.​1007/​s00294-015-0504-z PubMed
  Gosink KK, Mann ER, Guglielmo C, Tuomanen EI, Masure HR (2000) Role of novel choline binding proteins in virulence of Streptococcus pneumoniae. Infect Immun 68:5690–5695PubMedCentral CrossRef PubMed
  Greene NG, Narciso AR, Filipe SR, Camilli A (2015) Peptidoglycan branched stem peptides contribute to Streptococcus pneumoniae virulence by inhibiting pneumolysin release. PLoS Pathog 11:e1004996. doi:10.​1371/​journal.​ppat.​1004996 PubMedCentral CrossRef PubMed
  Guiral S, Mitchell TJ, Martin B, Claverys JP (2005) Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc Natl Acad Sci USA 102:8710–8715. doi:10.​1073/​pnas.​0500879102 PubMedCentral CrossRef PubMed
  Hava DL, Camilli A (2002) Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol 45:1389–1406PubMedCentral PubMed
  Hiller NL, Ahmed A, Powell E, Martin DP, Eutsey R, Earl J, Janto B, Boissy RJ, Hogg J, Barbadora K, Sampath R, Lonergan S, Post JC, Hu FZ, Ehrlich GD (2010) Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog 6:e1001108. doi:10.​1371/​journal.​ppat.​1001108 PubMedCentral CrossRef PubMed
  Johnston C, Martin B, Fichant G, Polard P, Claverys JP (2014) Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol 12:181–196. doi:10.​1038/​nrmicro3199 CrossRef PubMed
  Kazmierczak MJ, Wiedmann M, Boor KJ (2005) Alternative sigma factors and their roles in bacterial virulence. Microbiol Mol Biol Rev 69:527–543. doi:10.​1128/​MMBR.​69.​4.​527-543.​2005 PubMedCentral CrossRef PubMed
  Lau GW, Haataja S, Lonetto M, Kensit SE, Marra A, Bryant AP, McDevitt D, Morrison DA, Holden DW (2001) A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol Microbiol 40:555–571CrossRef PubMed
  Laurenceau R, Krasteva PV, Diallo A, Ouarti S, Duchateau M, Malosse C, Chamot-Rooke J, Fronzes R (2015) Conserved Streptococcus pneumoniae spirosomes suggest a single type of transformation pilus in competence. PLoS Pathog 11:e1004835. doi:10.​1371/​journal.​ppat.​1004835 PubMedCentral CrossRef PubMed
  Martin B, Granadel C, Campo N, Henard V, Prudhomme M, Claverys JP (2010) Expression and maintenance of ComD-ComE, the two-component signal-transduction system that controls competence of Streptococcus pneumoniae. Mol Microbiol 75:1513–1528. doi:10.​1111/​j.​1365-2958.​2010.​07071.​x CrossRef PubMed
  Mirouze N, Berge MA, Soulet AL, Mortier-Barriere I, Quentin Y, Fichant G, Granadel C, Noirot-Gros MF, Noirot P, Polard P, Martin B, Claverys JP (2013) Direct involvement of DprA, the transformation-dedicated RecA loader, in the shut-off of pneumococcal competence. Proc Natl Acad Sci USA 110:E1035–E1044. doi:10.​1073/​pnas.​1219868110 PubMedCentral CrossRef PubMed
  Mortier-Barriere I, Velten M, Dupaigne P, Mirouze N, Pietrement O, McGovern S, Fichant G, Martin B, Noirot P, Le Cam E, Polard P, Claverys JP (2007) A key presynaptic role in transformation for a widespread bacterial protein: DprA conveys incoming ssDNA to RecA. Cell 130:824–836. doi:10.​1016/​j.​cell.​2007.​07.​038 CrossRef PubMed
  Peterson SN, Sung CK, Cline R, Desai BV, Snesrud EC, Luo P, Walling J, Li H, Mintz M, Tsegaye G, Burr PC, Do Y, Ahn S, Gilbert J, Fleischmann RD, Morrison DA (2004) Identification of competence pheromone responsive genes in Streptococcus pneumoniae by use of DNA microarrays. Mol Microbiol 51:1051–1070CrossRef PubMed
  Price KE, Camilli A (2009) Pneumolysin localizes to the cell wall of Streptococcus pneumoniae. J Bacteriol 191:2163–2168. doi:10.​1128/​JB.​01489-08 PubMedCentral CrossRef PubMed
  Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys JP (2006) Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 313:89–92. doi:10.​1126/​science.​1127912 CrossRef PubMed
  Slager J, Kjos M, Attaiech L, Veening JW (2014) Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 157:395–406. doi:10.​1016/​j.​cell.​2014.​01.​068 CrossRef PubMed
  Souza BM, Castro TL, Carvalho RD, Seyffert N, Silva A, Miyoshi A, Azevedo V (2014) sigma(ECF) factors of gram-positive bacteria: a focus on Bacillus subtilis and the CMNR group. Virulence 5:587–600. doi:10.​4161/​viru.​29514 PubMedCentral CrossRef PubMed
  Spreer A, Kerstan H, Bottcher T, Gerber J, Siemer A, Zysk G, Mitchell TJ, Eiffert H, Nau R (2003) Reduced release of pneumolysin by Streptococcus pneumoniae in vitro and in vivo after treatment with nonbacteriolytic antibiotics in comparison to ceftriaxone. Antimicrob Agents Chemother 47:2649–2654PubMedCentral CrossRef PubMed
  Suga S, Chang B, Asada K, Akeda H, Nishi J, Okada K, Wakiguchi H, Maeda A, Oda M, Ishiwada N, Saitoh A, Oishi T, Hosoya M, Togashi T, Oishi K, Ihara T (2015) Nationwide population-based surveillance of invasive pneumococcal disease in Japanese children: effects of the seven-valent pneumococcal conjugate vaccine. Vaccine. doi:10.​1016/​j.​vaccine.​2015.​07.​069
  Tuchscherr L, Loffler B (2015) Staphylococcus aureus dynamically adapts global regulators and virulence factor expression in the course from acute to chronic infection. Curr Genet. doi:10.​1007/​s00294-015-0503-0 PubMed
  van der Linden M, Perniciaro S, Imohl M (2015) Increase of serotypes 15A and 23B in IPD in Germany in the PCV13 vaccination era. BMC Infect Dis 15:207. doi:10.​1186/​s12879-015-0941-9 PubMedCentral CrossRef PubMed
  Vorkapic D, Pressler K, Schild S (2015) Multifaceted roles of extracellular DNA in bacterial physiology. Curr Genet. doi:10.​1007/​s00294-015-0514-x PubMed
  Weng L, Piotrowski A, Morrison DA (2013) Exit from competence for genetic transformation in Streptococcus pneumoniae is regulated at multiple levels. PLoS One 8:e64197. doi:10.​1371/​journal.​pone.​0064197 PubMedCentral CrossRef PubMed
  Zhu L, Lau GW (2013) Therapeutic potential of the Streptococcus pneumoniae competence regulon. Expert Rev Anti Infect Ther 11:227–229. doi:10.​1586/​eri.​13.​10 CrossRef PubMed
  Zhu L, Kuang Z, Wilson BA, Lau GW (2013) Competence-independent activity of pneumococcal EndA mediates degradation of extracellular DNA and NETs and is important for virulence. PLoS One 8:e70363. doi:10.​1371/​journal.​pone.​0070363 PubMedCentral CrossRef PubMed
  Zhu L, Lin J, Kuang Z, Vidal JE, Lau GW (2015) Deletion analysis of Streptococcus pneumoniae late competence genes distinguishes virulence determinants that are dependent or independent of competence induction. Mol Microbiol 97:151–165. doi:10.​1111/​mmi.​13016 CrossRef PubMed
  
• 作者单位：Jingjun Lin (1)
  Luchang Zhu (1) (2)
  Gee W. Lau (1)
  
  1. Department of Pathobiology, University of Illinois at Urbana-Champaign, Urbana, IL, USA
  2. Department of Pathology and Genomic Medicine, Houston Methodist Hospital, Houston, TX, USA
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Microbial Genetics and Genomics
  Microbiology
  Biochemistry
  Cell Biology
  Plant Sciences
  Proteomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0983

文摘

Horizontal gene transfer mediated by the competence regulon is a major driver of genome plasticity in Streptococcus pneumoniae. When pneumococcal cells enter the competent state, about 6 % of the genes in the genome are up-regulated. Among these, some genes are essential for genetic transformation while others are dispensable for the process. Exhaustive deletion analyses show that some up-regulated genes dispensable for genetic transformation contribute to pneumococcal-mediated pneumonia and bacteremia infections. Interestingly, virulence functions of such genes are either dependent or independent of the competent state. Among the competent-state-dependent genes are those mediating allolysis, a process where small fraction of non-competent cells within the pneumococcal population are lysed by their competent counterparts, releasing DNA presumably for transformation. Inadvertently, the pore-forming toxin pneumolysin is also released during allolysis, contributing to virulence. In this review, we discuss recent advances in our understanding of pneumococcal virulence processes mediated by the competence regulon. We proposed that coupling of competence induction and bacterial fitness drives the natural selection to favor an intact competence regulon, which in turn, provides the long-term benefits of genetic plasticity. Keywords Streptococcus pneumoniae Competence Virulence Allolysis Pneumolysin