The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis.

The nosocomial human pathogen Moraxella catarrhalis is one the most important agents of human respiratory tract infections. This species is composed of two distinct lineages, one of only moderate virulence, the so-called serosensitive subpopulation, and a second, the seroresistant one, which is enriched among strains that harbor two major virulence traits: complement resistance and adherence to epithelial cells. Using a suite of population genetics tools, we show that the seroresistant lineage is also characterized by higher homologous recombination and mutation rates at housekeeping genes relative to its less pathogenic counterpart. Thus, sex and virulence have evolved in tandem in M. catarrhalis. Moreover, phylogenetic and Bayesian analyses that take into account recombination between the two clades show that the ancestral group was avirulent, is possibly 70 million years old, and must have infected mammals prior to the evolution of humans, which occurred later. The younger seroresistant isolates went through an important population expansion some 5 million years ago, coincident with the hominid expansion. This rise and spread was possibly coupled with a host shift and the acquisition of virulence genes.

[1]  Daniel Falush,et al.  An African origin for the intimate association between humans and Helicobacter pylori , 2007, Nature.

[2]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[3]  M. Maiden Multilocus sequence typing of bacteria. , 2006, Annual review of microbiology.

[4]  Daniel Falush,et al.  Sex and virulence in Escherichia coli: an evolutionary perspective , 2006, Molecular microbiology.

[5]  Liqing Zhang,et al.  Human SNPs reveal no evidence of frequent positive selection. , 2005, Molecular biology and evolution.

[6]  E. Denamur,et al.  Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection pathogenesis. , 2005, FEMS immunology and medical microbiology.

[7]  G. Syrogiannopoulos,et al.  Moraxella catarrhalis strains with reduced expression of the UspA outer membrane proteins belong to a distinct subpopulation. , 2005, Vaccine.

[8]  H. Ochman,et al.  Evolution in bacteria: Evidence for a universal substitution rate in cellular genomes , 1987, Journal of Molecular Evolution.

[9]  Giovanna Morelli,et al.  Microevolution and history of the plague bacillus, Yersinia pestis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Tim Brown,et al.  Silent Nucleotide Polymorphisms and a Phylogeny for Mycobacterium tuberculosis , 2004, Emerging infectious diseases.

[11]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[12]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[13]  M. Stephens,et al.  Traces of Human Migrations in Helicobacter pylori Populations , 2003, Science.

[14]  C. Aebi,et al.  Salivary Antibodies Directed against Outer Membrane Proteins of Moraxella catarrhalis in Healthy Adults , 2003 .

[15]  Yong Wang,et al.  An index of substitution saturation and its application. , 2003, Molecular phylogenetics and evolution.

[16]  Andrew Rambaut,et al.  GENIE: estimating demographic history from molecular phylogenies , 2002, Bioinform..

[17]  Tanja Popovic,et al.  Mutator clones of Neisseria meningitidis in epidemic serogroup A disease , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  P. Fearnhead,et al.  A coalescent-based method for detecting and estimating recombination from gene sequences. , 2002, Genetics.

[19]  A. van Belkum,et al.  Moraxella catarrhalis: from Emerging to Established Pathogen , 2002, Clinical Microbiology Reviews.

[20]  D. Falush,et al.  Recombination and mutation during long-term gastric colonization by Helicobacter pylori: Estimates of clock rates, recombination size, and minimal age , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  K. Strimmer,et al.  Exploring the demographic history of DNA sequences using the generalized skyline plot. , 2001, Molecular biology and evolution.

[22]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[23]  X. Xia,et al.  DAMBE: software package for data analysis in molecular biology and evolution. , 2001, The Journal of heredity.

[24]  E. Holmes,et al.  Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  B. Spratt,et al.  Recombination and the population structures of bacterial pathogens. , 2001, Annual review of microbiology.

[26]  T. Johnson,et al.  The evolution of mutation rates: separating causes from consequences , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  François Taddei,et al.  Evolutionary Implications of the Frequent Horizontal Transfer of Mismatch Repair Genes , 2000, Cell.

[28]  R. Lenski,et al.  The population genetics of ecological specialization in evolving Escherichia coli populations , 2000, Nature.

[29]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[30]  A. Oliver,et al.  High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. , 2000, Science.

[31]  F. Mooi,et al.  Analysis of Moraxella catarrhalis by DNA typing: evidence for a distinct subpopulation associated with virulence traits. , 2000, The Journal of infectious diseases.

[32]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[33]  J. Hacker,et al.  Pathogenicity islands and the evolution of microbes. , 2000, Annual review of microbiology.

[34]  L. Excoffier,et al.  Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. , 1999, Genetics.

[35]  Dexiang Chen,et al.  The Levels and Bactericidal Capacity of Antibodies Directed against the UspA1 and UspA2 Outer Membrane Proteins ofMoraxella (Branhamella) catarrhalis in Adults and Children , 1999, Infection and Immunity.

[36]  E. Hansen,et al.  Phenotypic Effect of Isogenic uspA1 anduspA2 Mutations on Moraxella catarrhalis 035E , 1998, Infection and Immunity.

[37]  S T Sherry,et al.  Genetic traces of ancient demography. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[38]  T. Murphy Lung infections. 2. Branhamella catarrhalis: epidemiological and clinical aspects of a human respiratory tract pathogen. , 1998, Thorax.

[39]  T. Logtenberg,et al.  Phage Antibodies Obtained by Competitive Selection on Complement-Resistant Moraxella (Branhamella)catarrhalis Recognize the High-Molecular-Weight Outer Membrane Protein , 1998, Infection and Immunity.

[40]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[41]  M. Ronaghi,et al.  Phylogeny of the family Moraxellaceae by 16S rDNA sequence analysis, with special emphasis on differentiation of Moraxella species. , 1998, International journal of systematic bacteriology.

[42]  F. Taddei,et al.  To be a mutator, or how pathogenic and commensal bacteria can evolve rapidly. , 1997, Trends in microbiology.

[43]  Y. Fu,et al.  Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. , 1997, Genetics.

[44]  F. Taddei,et al.  Role of mutator alleles in adaptive evolution , 1997, Nature.

[45]  M. Enright,et al.  Moraxella (Branhamella) catarrhalis--clinical and molecular aspects of a rediscovered pathogen. , 1997, Journal of medical microbiology.

[46]  T. Cebula,et al.  Hypermutability and homeologous recombination: Ingredients for rapid evolution , 1997 .

[47]  W. L. Payne,et al.  High Mutation Frequencies Among Escherichia coli and Salmonella Pathogens , 1996, Science.

[48]  H. Masaadeh,et al.  Neonatal meningitis due to Moraxella catarrhalis and review of the literature. , 1996, Annals of Tropical Paediatrics.

[49]  A. Rogers GENETIC EVIDENCE FOR A PLEISTOCENE POPULATION EXPLOSION , 1995, Evolution; international journal of organic evolution.

[50]  J. Verhoef,et al.  Assessment of complement-mediated killing of Moraxella (Branhamella) catarrhalis isolates by a simple method , 1995, Clinical and diagnostic laboratory immunology.

[51]  E. Hansen,et al.  A mutation affecting expression of a major outer membrane protein of Moraxella catarrhalis alters serum resistance and survival in vivo. , 1993, The Journal of infectious diseases.

[52]  J. M. Smith,et al.  How clonal are bacteria? , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. Enright,et al.  Outbreak of Moraxella catarrhalis in a respiratory unit. , 1993, Thorax.

[54]  J. Dorca,et al.  Branhamella catarrhalis respiratory infections. , 1992, The European respiratory journal.

[55]  B. Catlin Branhamella catarrhalis: an organism gaining respect as a pathogen , 1990, Clinical Microbiology Reviews.

[56]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[57]  M. Zervos,et al.  A nosocomial outbreak of Branhamella catarrhalis confirmed by restriction endonuclease analysis. , 1988, The Journal of infectious diseases.

[58]  M. Roberts,et al.  Branhamella (Neisseria) catarrhalis--a lower respiratory tract pathogen? , 1981, Journal of clinical microbiology.

[59]  K. Jyssum Mutator Factor in Neisseria meningitidis Associated with Increased Sensitivity to Ultraviolet Light and Defective Transformation , 1968, Journal of bacteriology.