Skip to main content Accessibility help
×
Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-09T20:37:38.618Z Has data issue: false hasContentIssue false

9 - Genomic or Pathogenicity Islands in Streptococcus pneumoniae

from PART III - Paradigms of Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
Get access

Summary

INTRODUCTION

Bacterial genomes are no longer considered a stable and rigid DNA structure carrying the essential genetic information for survival, fitness, and transmission of the species. With the development of genomic high-throughput techniques such as sequencing of whole bacterial genomes (with a total in November 2007 of 597 complete microbial genomes that are sequenced and 879 genomes in progress; http://www.ncbi.nlm.nih.gov/genomes/lproks.cgi) and the bioinformatics tools, our view of bacterial genome plasticity has changed. Bacterial genomes are now regarded as highly flexible and dynamic structures that change in size, genetic content, and organization over time (Hanage et al., 2006). This flexibility is also known as genome evolution (Groisman and Casadesus, 2005). It is thought that this evolution is driven by the adaptation of microorganisms to environmental niches, changes, or stresses and occurs via several mechanisms including point mutations, deletions, and gene acquisition/loss via horizontal gene transfer (Albiger et al., 1999; Chen et al., 2005). This latter process is associated with mobile genetic elements such as conjugative plasmids, bacteriophages, transposons, insertion sequence (IS) elements, and genomic islands (Albiger et al., 1999; Frost et al., 2005).

In Gram-negative bacteria, pathogenicity islands (PAI) are genomic regions that harbor one or more gene clusters encoding virulence-associated properties (reviewed in Gal-Mor and Finlay, 2006; Schmidt and Hensel, 2004). They are present in the genomes of pathogenic bacteria and usually absent from the same or closely related non-pathogenic species.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albiger, B., Hubert, J. C., and Lett, M. C. (1999). Identification of the plasmid-mobilization potential of the strain Klebsiella pneumoniae ozenae KIIIA isolated from a polluted aquatic environment. Plasmid, 41, 30–9.CrossRefGoogle ScholarPubMed
Albiger, B., Sandgren, A., Katsuragi, H., et al. (2005). Myeloid differentiation factor 88-dependent signalling controls bacterial growth during colonization and systemic pneumococcal disease in mice. Cell Microbiol, 7, 1603–15.CrossRefGoogle ScholarPubMed
Albiger, B., Dahlberg, S., Sandgren, A., et al. (2006). Toll-like receptor 9 acts at an early stage in host defence against pneumococcal infection. Cell Microbiol, 9, 633–44.CrossRefGoogle ScholarPubMed
Barocchi, M. A., Ries, J., Zogaj, X., et al. (2006). A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA, 103, 2857–62.CrossRefGoogle ScholarPubMed
Beall, B., McEllistrem, M. C., Gertz, R. E., et al. (2006). Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002. J Clin Microbiol, 44, 999–1017.CrossRefGoogle ScholarPubMed
Bensing, B. A., Lopez, J. A., and Sullam, P. M. (2004). The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Iba. Infect Immun, 72, 6528–37.CrossRefGoogle Scholar
Bentley, S. D., Aanensen, D. M., Mavroidi, A., et al. (2006). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet, 2, e31.CrossRefGoogle ScholarPubMed
Blue, C. E., Paterson, G. K., Kerr, A. R., et al. (2003). ZmpB, a novel virulence factor of Streptococcus pneumoniae that induces tumor necrosis factor alpha production in the respiratory tract. Infect Immun, 71, 4925–35.CrossRefGoogle ScholarPubMed
Bogaert, D., Groot, R., and Hermans, P. W. (2004). Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis, 4, 144–54.CrossRefGoogle ScholarPubMed
Brown, J. S., and Holden, D. W. (2002). Iron acquisition by Gram-positive bacterial pathogens. Microb Infect, 4, 1149–56.CrossRefGoogle ScholarPubMed
Brown, J. S., Gilliland, S. M., and Holden, D. W. (2001). A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol Microbiol, 40, 572–85.CrossRefGoogle ScholarPubMed
Brown, J. S., Gilliland, S. M., Ruiz-Albert, J., and Holden, D. W. (2002). Characterization of pit, a Streptococcus pneumoniae iron uptake ABC transporter. Infect Immun, 70, 4389–98.CrossRefGoogle ScholarPubMed
Brown, J. S., Gilliland, S. M., Basavanna, S., et al. (2004a). phgABC, a three-gene operon required for growth of Streptococcus pneumoniae in hyperosmotic medium and in vivo. Infect Immun, 72, 4579–88.CrossRefGoogle ScholarPubMed
Brown, J. S., Gilliland, S. M., Spratt, B. G., and Holden, D. W. (2004b), A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infect Immun, 72, 1587–93.CrossRefGoogle ScholarPubMed
Bruckner, R., Nuhn, M., Reichmann, P., Weber, B., and Hakenbeck, R. (2004) Mosaic genes and mosaic chromosomes-genomic variation in Streptococcus pneumoniae. Int J Med Microbiol, 294, 157–68.CrossRefGoogle ScholarPubMed
Brueggemann, A. B., and Spratt, B. G. (2003). Geographic distribution and clonal diversity of Streptococcus pneumoniae serotype 1 isolates. J Clin Microbiol, 41, 4966–70.CrossRefGoogle ScholarPubMed
Brueggemann, A. B., Griffiths, D. T., Meats, E., et al. (2003). Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis, 187, 1424–32.CrossRefGoogle ScholarPubMed
Brueggemann, A. B., Peto, T. E., Crook, D. W., et al. (2004). Temporal and geographic stability of the serogroup-specific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis, 190, 1203–11.CrossRefGoogle ScholarPubMed
Burne, R. A. (1998). Oral streptococci … products of their environment. J Dent Res, 77, 445–52.CrossRefGoogle Scholar
Camilli, R., Pettini, E., Grosso, M. D., et al. (2006). Zinc metalloproteinase genes in clinical isolates of Streptococcus pneumoniae: association of the full array with a clonal cluster comprising serotypes 8 and 11A. Microbiology, 152, 313–21.CrossRefGoogle ScholarPubMed
Chen, I., Christie, P. J., and Dubnau, D. (2005). The ins and outs of DNA transfer in bacteria. Science, 310, 1456–60.CrossRefGoogle ScholarPubMed
Chiavolini, D., Memmi, G., Maggi, T., et al. (2003). The three extra-cellular zinc metalloproteinases of Streptococcus pneumoniae have a different impact on virulence in mice. BMC Microbiol, 3, 14.CrossRefGoogle ScholarPubMed
Claverys, J. P., and Havarstein, L. S. (2002). Extracellular-peptide control of competence for genetic transformation in Streptococcus pneumoniae. Front Biosci, 7, d1798–814.CrossRefGoogle ScholarPubMed
Claverys, J. P., Prudhomme, M., Mortier-Barriere, I., and Martin, B. (2000). Adaptation to the environment: Streptococcus pneumoniae, a paradigm for recombination-mediated genetic plasticity?Mol Microbiol, 35, 251–9.CrossRefGoogle ScholarPubMed
Coffey, T. J., Enright, M. C., Daniels, M., et al. (1998a). Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae. Mol Microbiol, 27, 73–83.CrossRefGoogle ScholarPubMed
Coffey, T. J., Enright, M. C., Daniels, M., et al. (1998b). Serotype 19A variants of the Spanish serotype 23F multiresistant clone of Streptococcus pneumoniae. Microb Drug Resist, 4, 51–5.CrossRefGoogle ScholarPubMed
Coffey, T. J., Daniels, M., Enright, M. C., and Spratt, B. G. (1999). Serotype 14 variants of the Spanish penicillin-resistant serotype 9V clone of Streptococcus pneumoniae arose by large recombinational replacements of the cpsA-pbp1a region. Microbiology, 145, 2023–31.CrossRefGoogle ScholarPubMed
Dramsi, S., Caliot, E., Bonne, I., et al. (2006). Assembly and role of pili in group B streptococci. Mol Microbiol, 60, 1401–13.CrossRefGoogle ScholarPubMed
Enright, M. C., and Spratt, B. G. (1998). A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology, 144, 3049–60.CrossRefGoogle ScholarPubMed
Enright, M. C., and Spratt, B. G. (1999). Multilocus sequence typing. Trends Microbiol, 7, 482–7.CrossRefGoogle ScholarPubMed
Frost, L. S., Leplae, R., Summers, A. O., and Toussaint, A. (2005). Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol, 3, 722–32.CrossRefGoogle ScholarPubMed
Gal-Mor, O., and Finlay, B. B. (2006). Pathogenicity islands: a molecular toolbox for bacterial virulence. Cell Microbiol, 8, 1707–19.CrossRefGoogle ScholarPubMed
Gaspar, A. H., and Ton-That, H. (2006). Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae. J Bacteriol, 188, 1526–33.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Casadesus, J. (2005). The origin and evolution of human pathogens. Mol Microbiol, 56, 1–7.CrossRefGoogle ScholarPubMed
Hakenbeck, R., Balmelle, N., Weber, B., et al. (2001). Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect Immun, 69, 2477–86.CrossRefGoogle ScholarPubMed
Hanage, W. P., Kaijalainen, T., Herva, E., et al. (2005). Using multilocus sequence data to define the pneumococcus. J Bacteriol, 187, 6223–30.CrossRefGoogle ScholarPubMed
Hanage, W. P., Fraser, C., and Spratt, B. G. (2006). The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol, 239, 210–9.CrossRefGoogle ScholarPubMed
Hausdorff, W. P. (2002). Invasive pneumococcal disease in children: geographic and temporal variations in incidence and serotype distribution. Eur J Pediatr, 161(Suppl 2), S135–9.CrossRefGoogle Scholar
Hausdorff, W. P., Siber, G., and Paradiso, P. R. (2001). Geographical differences in invasive pneumococcal disease rates and serotype frequency in young children. Lancet, 357, 950–2.CrossRefGoogle ScholarPubMed
Hausdorff, W. P., Yothers, G., Dagan, R., et al. (2002). Multinational study of pneumococcal serotypes causing acute otitis media in children. Pediatr Infect Dis J, 21, 1008–16.CrossRefGoogle ScholarPubMed
Hausdorff, W. P., Feikin, D. R., and Klugman, K. P. (2005). Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis, 5, 83–93.CrossRefGoogle ScholarPubMed
Hava, D. L., and Camilli, A. (2002). Large-scale identification of serotype 4 Streptococcus pneumoniae virulence factors. Mol Microbiol, 45, 1389–406.Google ScholarPubMed
Hava, D. L., Hemsley, C. J., and Camilli, A. (2003a). Transcriptional regulation in the Streptococcus pneumoniae rlrA pathogenicity islet by RlrA. J Bacteriol, 185, 413–21.CrossRefGoogle ScholarPubMed
Hava, D. L., LeMieux, J., and Camilli, A. (2003b). From nose to lung: the regulation behind Streptococcus pneumoniae virulence factors. Mol Microbiol, 50, 1103–10.CrossRefGoogle ScholarPubMed
Hemsley, C., Joyce, E., Hava, D. L., Kawale, A., and Camilli, A. (2003). MgrA, an orthologue of Mga, acts as a transcriptional repressor of the genes within the rlrA pathogenicity islet in Streptococcus pneumoniae. J Bacteriol, 185, 6640–7.CrossRefGoogle ScholarPubMed
Henriques, B., Kalin, M., Ortqvist, A., et al. (2000). Molecular epidemiology of Streptococcus pneumoniae causing invasive disease in 5 countries. J Infect Dis, 182, 833–9.CrossRefGoogle ScholarPubMed
Henriques-Normark, B., Kalin, M., Ortqvist, A., et al. (2001). Dynamics of penicillin-susceptible clones in invasive pneumococcal disease. J Infect Dis, 184, 861–9.CrossRefGoogle ScholarPubMed
Henriques-Normark, B., Christensson, B., Sandgren, A., et al. (2003). Clonal analysis of Streptococcus pneumoniae nonsusceptible to penicillin at day-care centers with index cases, in a region with low incidence of resistance: emergence of an invasive type 35B clone among carriers. Microb Drug Resist, 9, 337–44.CrossRefGoogle Scholar
Herzberg, M. C., Meyer, M. W., Kilic, A., and Tao, L. (1997). Host-pathogen interactions in bacterial endocarditis: streptococcal virulence in the host. Adv Dent Res, 11, 69–74.CrossRefGoogle Scholar
Hoskins, J., Alborn, W. E., Arnold, J., et al. (2001). Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol, 183, 5709–17.CrossRefGoogle ScholarPubMed
Jakubovics, N. S., Kerrigan, S. W., Nobbs, A. H., et al. (2005). Functions of cell surface-anchored antigen I/II family and Hsa polypeptides in interactions of Streptococcus gordonii with host receptors. Infect Immun, 73, 6629–38.CrossRefGoogle ScholarPubMed
Kan, B., Ries, J., Normark, B. H., et al. (2006). Endocarditis and pericarditis complicating pneumococcal bacteraemia, with special reference to the adhesive abilities of pneumococci: results from a prospective study. Clin Microbiol Infect, 12, 338–44.CrossRefGoogle ScholarPubMed
Kilian, M., Reinholdt, J., Lomholt, H., Poulsen, K., and Frandsen, E. V. (1996) Biological significance of IgA1 proteases in bacterial colonization and pathogenesis: critical evaluation of experimental evidence. APMIS, 104, 321–38.CrossRefGoogle ScholarPubMed
King, S. J., Hippe, K. R., and Weiser, J. N. (2006). Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol, 59, 961–74.CrossRefGoogle ScholarPubMed
Knutsen, E., Johnsborg, O., Quentin, Y.Claverys, J. P., and Havarstein, L. S. (2006). BOX-elements modulate gene expression in Streptococcus pneumoniae: impact on the fine-tuning of competence development. J Bacteriol, 88, 8307–12.CrossRefGoogle Scholar
Kyaw, M. H., Lynfield, R., Schaffner, W., et al. (2006). Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med, 354, 1455–63.CrossRefGoogle ScholarPubMed
Lanie, J. A., Ng, W. L., Kazmierczak, K. M., Andrzejewski, T. M., et al. (2007). Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol, 189, 38-51.CrossRefGoogle ScholarPubMed
Lauer, P., Rinaudo, C. D., Soriani, M., et al. (2005). Genome analysis reveals pili in Group B Streptococcus. Science, 309, 105.CrossRefGoogle ScholarPubMed
LeMieux, J., Hava, D. L., Basset, A., and Camilli, A. (2006). RrgA and RrgB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae rlrA pathogenicity islet. Infect Immun, 74, 2453–6.CrossRefGoogle ScholarPubMed
Manco, S., Hernon, F., Yesilkaya, H., et al. (2006). Pneumococcal neuraminidases A and B both have essential roles during infection of the respiratory tract and sepsis. Infect Immun, 74, 4014–20.CrossRefGoogle Scholar
Martens, P., Worm, S. W., Lundgren, B., Konradsen, H. B., and Benfield, T. (2004). Serotype-specific mortality from invasive Streptococcus pneumoniae disease revisited. BMC Infect Dis, 4, 21.CrossRefGoogle ScholarPubMed
McCoy, S., and Pettigrew, M. (2003). Molecular epidemiology of Streptococcus pneumoniae mediated otitis media. Front Biosci, 8, e87–93.Google ScholarPubMed
Meats, E., Brueggemann, A. B., Enright, M. C., et al. (2003). Stability of serotypes during nasopharyngeal carriage of Streptococcus pneumoniae. J Clin Microbiol, 41, 386–92.CrossRefGoogle ScholarPubMed
Mora, M., Bensi, G., Capo, S., et al. (2005). Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA, 102, 15641–6.CrossRefGoogle ScholarPubMed
Nallapareddy, S. R., Singh, K. V., Sillanpaa, J., et al. (2006). Endocarditis and biofilm-associated pili of Enterococcus faecalis. J Clin Invest, 116, 2799–807.CrossRefGoogle ScholarPubMed
Obert, C., Sublett, J., Kaushal, D., et al. (2006). Identification of a candidate Streptococcus pneumoniae core genome and regions of diversity correlated with invasive pneumococcal disease. Infect Immun, 74, 4766–77.CrossRefGoogle ScholarPubMed
Oggioni, M. R., and Claverys, J. P. (1999). Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology, 145, 2647–53.CrossRefGoogle ScholarPubMed
Oggioni, M. R., Memmi, G., Maggi, T., et al. (2003). Pneumococcal zinc metalloproteinase ZmpC cleaves human matrix metalloproteinase 9 and is a virulence factor in experimental pneumonia. Mol Microbiol, 49, 795–805.CrossRefGoogle ScholarPubMed
Orihuela, C. J., Gao, G., Mcgee, M., et al. (2003). Organ-specific models of Streptococcus pneumoniae disease. Scand J Infect Dis, 35, 647–52.CrossRefGoogle ScholarPubMed
Orihuela, C. J., Gao, G., Francis, K. P., et al. (2004a). Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J Infect Dis, 190, 1661–9.CrossRefGoogle ScholarPubMed
Orihuela, C. J., Radin, J. N., Sublett, J. E., Yu, J., and Tuomanen, E. I. (2004b). Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun, 72, 5582–96.CrossRefGoogle ScholarPubMed
Paterson, N. G., Riboldi-Tunicliffe, A., Mitchell, T. J., and Isaacs, N. W. (2006). Overexpression, purification and crystallization of a choline-binding protein CbpI from Streptococcus pneumoniae. Acta Crystallogr Sect F Struct Biol Cryst Commun, 62, 672–5.CrossRefGoogle ScholarPubMed
Pebody, R. G., Leino, T., Nohynek, H., et al. (2005). Pneumococcal vaccination policy in Europe. Eur Surveill, 10, 174–8.CrossRefGoogle Scholar
Pettigrew, M. M., and Fennie, K. P. (2005). Genomic subtraction followed by dot blot screening of Streptococcus pneumoniae clinical and carriage isolates identifies genetic differences associated with strains that cause otitis media. Infect Immun, 73, 2805–11.CrossRefGoogle ScholarPubMed
Pettigrew, M. M., Fennie, K. P., York, M. P., Daniels, J., and Ghaffar, F. (2006). Variation in the presence of neuraminidase genes among Streptococcus pneumoniae isolates with identical sequence types. Infect Immun, 74, 3360–5.CrossRefGoogle ScholarPubMed
Rosini, R., Rinaudo, C. D., Soriani, M., et al. (2006). Identification of novel genomic islands coding for antigenic pilus-like structures in Streptococcus agalactiae. Mol Microbiol, 61, 126–41.CrossRefGoogle ScholarPubMed
Sandgren, A., Sjostrom, K., Olsson-Liljequist, B., et al. (2004). Effect of clonal and serotype-specific properties on the invasive capacity of Streptococcus pneumoniae. J Infect Dis, 189, 785–96.CrossRefGoogle ScholarPubMed
Sandgren, A., Albiger, B., Orihuela, C. J., et al. (2005). Virulence in mice of pneumococcal clonal types with known invasive disease potential in humans. J Infect Dis, 192, 791–800.CrossRefGoogle ScholarPubMed
Schmidt, H., and Hensel, M. (2004). Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev, 17, 14–56.CrossRefGoogle ScholarPubMed
Scott, J. R., and Zahner, D. (2006). Pili with strong attachments: Gram-positive bacteria do it differently. Mol Microbiol, 62, 320–30.CrossRefGoogle ScholarPubMed
Shakhnovich, E. A., King, S. J., and Weiser, J. N. (2002). Neuraminidase expressed by Streptococcus pneumoniae desialylates the lipopolysaccharide of Neisseria meningitidis and Haemophilus influenzae: a paradigm for interbacterial competition among pathogens of the human respiratory tract. Infect Immun, 70, 7161–4.CrossRefGoogle ScholarPubMed
Silva, N. A., McCluskey, J., Jefferies, J. M., et al. (2006). Genomic diversity between strains of the same serotype and multilocus sequence type among pneumococcal clinical isolates. Infect Immun, 74, 3513–8.CrossRefGoogle ScholarPubMed
Sjostrom, K., Spindler, C., Ortqvist, A., et al. (2006). Clonal and capsular types decide whether pneumococci will act as a primary or opportunistic pathogen. Clin Infect Dis, 42, 451–9.CrossRefGoogle ScholarPubMed
Sjostrom, K., Blomberg, C., Fernebro, J., et al. (2007). Clonal success of piliated penicillin nonsusceptible pneumococci. Proc Natl Acad Sci USA, 104, 12907–12.CrossRefGoogle ScholarPubMed
Tai, S. S. (2006). Streptococcus pneumoniae protein vaccine candidates: properties, activities and animal studies. Crit Rev Microbiol, 32, 139–53.CrossRefGoogle ScholarPubMed
Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2004). Four proteins encoded in the gspB-secY2A2 operon of Streptococcus gordonii mediate the intracellular glycosylation of the platelet-binding protein GspB. J Bacteriol, 186, 7100–11.CrossRefGoogle ScholarPubMed
Takamatsu, D., Bensing, B. A., Cheng, H., et al. (2005a). Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibα. Mol Microbiol, 58, 380–92.CrossRefGoogle ScholarPubMed
Takamatsu, D., Bensing, B. A., and Sullam, P. M. (2005b). Two additional components of the accessory sec system mediating export of the Streptococcus gordonii platelet-binding protein GspB. J Bacteriol, 187, 3878–83.CrossRefGoogle ScholarPubMed
Takamatsu, D., Bensing, B. A., Prakobphol, A., Fisher, S. J., and Sullam, P. M. (2006). Binding of the streptococcal surface glycoproteins GspB and Hsa to human salivary proteins. Infect Immun, 74, 1933–40.CrossRefGoogle ScholarPubMed
Telford, J. L., Barocchi, M. A., Margarit, I., Rappuoli, R., and Grandi, G. (2006). Pili in gram-positive pathogens. Nat Rev Microbiol, 4, 509–19.CrossRefGoogle ScholarPubMed
Tettelin, H., Nelson, K. E., Paulsen, I. T., et al. (2001). Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science, 293, 498–506.CrossRefGoogle ScholarPubMed
Wani, J. H., Gilbert, J. V., Plaut, A. G., and Weiser, J. N. (1996). Identification, cloning, and sequencing of the immunoglobulin A1 protease gene of Streptococcus pneumoniae. Infect Immun, 64, 3967–74.Google ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×