Rapid Pneumococcal Evolution in Response to Clinical Interventions

Streptococcus pneumonia evades vaccines and drugs by high levels of recombination and rapid adaptation. Epidemiological studies of the naturally transformable bacterial pathogen Streptococcus pneumoniae have previously been confounded by high rates of recombination. Sequencing 240 isolates of the PMEN1 (Spain23F-1) multidrug-resistant lineage enabled base substitutions to be distinguished from polymorphisms arising through horizontal sequence transfer. More than 700 recombinations were detected, with genes encoding major antigens frequently affected. Among these were 10 capsule-switching events, one of which accompanied a population shift as vaccine-escape serotype 19A isolates emerged in the USA after the introduction of the conjugate polysaccharide vaccine. The evolution of resistance to fluoroquinolones, rifampicin, and macrolides was observed to occur on multiple occasions. This study details how genomic plasticity within lineages of recombinogenic bacteria can permit adaptation to clinical interventions over remarkably short time scales.

[1]  Julian Parkhill,et al.  Evolution of MRSA During Hospital Transmission and Intercontinental Spread , 2010, Science.

[2]  Marc Lipsitch,et al.  What is the mechanism for persistent coexistence of drug-susceptible and drug-resistant strains of Streptococcus pneumoniae? , 2009, Journal of The Royal Society Interface.

[3]  T. Cherian,et al.  Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates , 2009, The Lancet.

[4]  D. Rolo,et al.  Emergence of a multidrug-resistant clone (ST320) among invasive serotype 19A pneumococci in Spain. , 2009, The Journal of antimicrobial chemotherapy.

[5]  Jukka Corander,et al.  Hyper-Recombination, Diversity, and Antibiotic Resistance in Pneumococcus , 2009, Science.

[6]  R. Reinert.  The public health ramifications of pneumococcal resistance. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[7]  R. Dagan.  Impact of pneumococcal conjugate vaccine on infections caused by antibiotic-resistant Streptococcus pneumoniae. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[8]  M. Quail,et al.  Role of Conjugative Elements in the Evolution of the Multidrug-Resistant Pandemic Clone Streptococcus pneumoniaeSpain23F ST81 , 2008, Journal of bacteriology.

[9]  R. Dagan,et al.  Impact of conjugate pneumococcal vaccines on antibiotic resistance. , 2008, The Lancet. Infectious diseases.

[10]  J. Wain,et al.  High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi , 2008, Nature Genetics.

[11]  C. Orihuela,et al.  Antibodies against PsrP, a novel Streptococcus pneumoniae adhesin, block adhesion and protect mice against pneumococcal challenge. , 2008, The Journal of infectious diseases.

[12]  W. Schaffner,et al.  Population snapshot of emergent Streptococcus pneumoniae serotype 19A in the United States, 2005. , 2008, The Journal of infectious diseases.

[13]  C. Muñoz-Almagro,et al.  Emergence of invasive pneumococcal disease caused by nonvaccine serotypes in the era of 7-valent conjugate vaccine. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[14]  A. Pantosti,et al.  The Macrolide Resistance Genes erm(B) and mef(E) Are Carried by Tn2010 in Dual-Gene Streptococcus pneumoniae Isolates Belonging to Clonal Complex CC271 , 2007, Antimicrobial Agents and Chemotherapy.

[15]  T. Mitchell,et al.  Isolation and characterization of a new plasmid pSpnP1 from a multidrug-resistant clone of Streptococcus pneumoniae. , 2007, Plasmid.

[16]  A. Pantosti,et al.  The mef(E)-Carrying Genetic Element (mega) of Streptococcus pneumoniae: Insertion Sites and Association with Other Genetic Elements , 2006, Antimicrobial Agents and Chemotherapy.

[17]  T. Welte,et al.  Fluoroquinolone-resistant Streptococcus pneumoniae , 2006, Emerging infectious diseases.

[18]  Julian Parkhill,et al.  Genetic Analysis of the Capsular Biosynthetic Locus from All 90 Pneumococcal Serotypes , 2006, PLoS genetics.

[19]  E. Cercenado,et al.  New Mutations and Horizontal Transfer of rpoB among Rifampin-Resistant Streptococcus pneumoniae from Four Spanish Hospitals , 2005, Antimicrobial Agents and Chemotherapy.

[20]  B. Spratt,et al.  Cluster of an erythromycin-resistant variant of the Spanish multiply resistant 23F clone ofStreptococcus pneumoniae in South Africa , 1994, European Journal of Clinical Microbiology and Infectious Diseases.

[21]  M. Lipsitch,et al.  Single-Step Capsular Transformation and Acquisition of Penicillin Resistance in Streptococcus pneumoniae , 2004, Journal of bacteriology.

[22]  T. Cate,et al.  Serum Immunoglobulin G Response to Candidate Vaccine Antigens during Experimental Human Pneumococcal Colonization , 2003, Infection and Immunity.

[23]  N. M. Duong,et al.  Emergence in Vietnam of Streptococcus pneumoniae Resistant to Multiple Antimicrobial Agents as a Result of Dissemination of the Multiresistant Spain23F-1 Clone , 2002, Antimicrobial Agents and Chemotherapy.

[24]  A. Tomasz,et al.  Nomenclature of Major Antimicrobial-Resistant Clones of Streptococcus pneumoniae Defined by the Pneumococcal Molecular Epidemiology Network , 2001, Journal of Clinical Microbiology.

[25]  J. M. Smith,et al.  Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. , 2000, Genetics.

[26]  N. Moran,et al.  Calibrating bacterial evolution. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[27]  D. Morrison,et al.  Isolation and Characterization of Three Streptococcus pneumoniae Transformation-Specific Loci by Use of alacZ Reporter Insertion Vector , 1998, Journal of bacteriology.

[28]  A. Tomasz,et al.  Molecular characterization of penicillin-resistant Streptococcus pneumoniae isolates causing respiratory disease in the United States. , 1998, Microbial drug resistance.

[29]  A. Tomasz,et al.  Spread of the serotype 23F multidrug-resistant Streptococcus pneumoniae clone to South Korea. , 1997, Microbial drug resistance.

[30]  L. McGee,et al.  Spread of the Spanish multi-resistant serotype 23F clone of Streptococcus pneumoniae to Seoul, Korea. , 1997, Microbial drug resistance.

[31]  A. Tomasz,et al.  Intercontinental spread of a multiresistant clone of serotype 23F Streptococcus pneumoniae. , 1991, The Journal of infectious diseases.

[32]  D. Clewell,et al.  Complete nucleotide sequence of macrolide-lincosamide-streptogramin B-resistance transposon Tn917 in Streptococcus faecalis , 1985, Journal of bacteriology.

[33]  A. Buu-Hoï,et al.  Conjugative transfer of multiple antibiotic resistance markers in Streptococcus pneumoniae , 1980, Journal of bacteriology.