Evolution of bacterial pathogenesis

Abstract. The evolution of bacteria is associated with continuous generation of novel genetic variants. The major driving forces in this process are point mutations, genetic rearrangements, and horizontal gene transfer. A large number of human and animal bacterial pathogens have evolved the capacity to produce virulence factors that are directly involved in infection and disease. Additionally, many bacteria express resistance traits against antibiotics. Both virulence factors and resistance determinants are subject to intrastrain genetic and phenotypic variation. They are often encoded on unstable DNA regions. Thus, they can be readily transferred to bacteria of the same species or even to non-related prokaryotes. This review article focuses on the main mechanisms of bacterial microevolution responsible for the rapid emergence of variants with novel virulence and resistance properties. In addition, processes of macroevolution are described with special emphasis on gene transfer and fixation of adaptive mutations in the genome of pathogens.

[1]  R M Hall,et al.  Mobile gene cassettes and integrons: capture and spread of genes by site‐specific recombination , 1995, Molecular microbiology.

[2]  James C. Paton,et al.  Pathogenesis and Diagnosis of Shiga Toxin-Producing Escherichia coli Infections , 1998, Clinical Microbiology Reviews.

[3]  M. Simon,et al.  Recombinational switch for gene expression. , 1977, Science.

[4]  H. Shinagawa,et al.  Processing the holliday junction in homologous recombination. , 1996, Trends in biochemical sciences.

[5]  Howard Ochman,et al.  Pathogenicity Islands: Bacterial Evolution in Quantum Leaps , 1996, Cell.

[6]  M. Hecker,et al.  Non‐specific, general and multiple stress resistance of growth‐restricted Bacillus subtilis cells by the expression of the σB regulon , 1998, Molecular microbiology.

[7]  J. Abraham,et al.  An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[8]  H. Sweeney,et al.  Effect of the Prophage and Penicillinase Plasmid of the Recipient Strain Upon the Transduction and the Stability of Methicillin Resistance in Staphylococcus aureus , 1973, Journal of bacteriology.

[9]  H. Seifert,et al.  Genetic mechanisms of bacterial antigenic variation. , 1988, Microbiological reviews.

[10]  J Hacker,et al.  Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution , 1997, Molecular microbiology.

[11]  Teruyo Ito,et al.  Cloning and Nucleotide Sequence Determination of the Entire mec DNA of Pre-Methicillin-Resistant Staphylococcus aureus N315 , 1999, Antimicrobial Agents and Chemotherapy.

[12]  M. Levine,et al.  A plasmid of enterohemorrhagic Escherichia coli O157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells , 1987, Infection and immunity.

[13]  H. Karch,et al.  A gene cluster closely related to type II secretion pathway operons of gram-negative bacteria is located on the large plasmid of enterohemorrhagic Escherichia coli O157 strains. , 1997, FEMS microbiology letters.

[14]  H. Chambers.  Methicillin resistance in staphylococci: molecular and biochemical basis and clinical implications , 1997, Clinical microbiology reviews.

[15]  D. Dykhuizen,et al.  Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Chandler,et al.  Insertion Sequences , 1998, Microbiology and Molecular Biology Reviews.

[17]  R. Hengge-aronis,et al.  Interplay of global regulators and cell physiology in the general stress response of Escherichia coli. , 1999, Current opinion in microbiology.

[18]  D. Sherratt,et al.  Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements. , 1997, FEMS microbiology reviews.

[19]  K. Schleifer,et al.  Specific Detection of Legionella pneumophila: Construction of a New 16S rRNA-Targeted Oligonucleotide Probe , 1998, Applied and Environmental Microbiology.

[20]  L. A. Lewis,et al.  The Non‐Random Pattern of Insertion of IS2 into the hemB Gene of Escherichia coli , 1994, Microbiology and immunology.

[21]  J. Hacker,et al.  Regulation of σB-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains , 1999, Molecular and General Genetics MGG.

[22]  H. Seifert.  Questions about gonococcal pilus phase‐ and antigenic variation , 1996, Molecular microbiology.

[23]  D. Dykhuizen,et al.  Pathoadaptive mutations: gene loss and variation in bacterial pathogens. , 1999, Trends in microbiology.

[24]  T. Meyer,et al.  Biology of the pathogenic Neisseriae. , 1994, Current topics in microbiology and immunology.

[25]  R. Hakenbeck,et al.  Resistant penicillin-binding proteins , 1998, Cellular and Molecular Life Sciences CMLS.

[26]  F. Fang,et al.  Central regulatory role for the RpoS sigma factor in expression of Salmonella dublin plasmid virulence genes , 1995, Journal of bacteriology.

[27]  D. Maneval,et al.  A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria , 1999, Nature.

[28]  R. Losick,et al.  Crisscross regulation of cell-type-specific gene expression during development in B. subtilis , 1992, Nature.

[29]  P. Sniegowski.  Mismatch repair: Origin of species? , 1998, Current Biology.

[30]  P. Klemm,et al.  Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. , 1986, The EMBO journal.

[31]  W. Winn,et al.  Legionnaires disease: historical perspective , 1988, Clinical Microbiology Reviews.

[32]  A. Häusler,et al.  Chromosomal deletion and rearrangement in Streptomyces glaucescens , 1991, Journal of bacteriology.

[33]  I. Kullik,et al.  Deletion of the Alternative Sigma Factor ςB in Staphylococcus aureus Reveals Its Function as a Global Regulator of Virulence Genes , 1998, Journal of bacteriology.

[34]  A. Tomasz.  Antibiotic resistance in Streptococcus pneumoniae. , 1997, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[35]  A. Tomasz,et al.  Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing , 1996, Journal of bacteriology.

[36]  I. Blomfield,et al.  Interaction of FimB and FimE with the fim switch that controls the phase variation of type 1 fimbriae in Escherichia coli K‐12 , 1996, Molecular microbiology.

[37]  D. Friedman.  Interaction between bacteriophage λ and its Escherichia coli host , 1992 .

[38]  R. Perry,et al.  Yersinia pestis--etiologic agent of plague , 1997, Clinical microbiology reviews.

[39]  M. Achtman.  Epidemic spread and antigenic variability of Neisseria meningitidis. , 1995, Trends in microbiology.

[40]  D. Gally,et al.  Regulation of type 1 fimbrial expression in uropathogenic Escherichia coli : heterogeneity of expression through sequence changes in the fim switch region , 1998, Molecular microbiology.

[41]  S. Hammerschmidt,et al.  Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. , 1996, The EMBO journal.

[42]  L. Rice,et al.  Transfer of Tn5385, a Composite, Multiresistance Chromosomal Element from Enterococcus faecalis , 1998, Journal of bacteriology.

[43]  M. Rupp.  Coagulase-negative staphylococcal infections: an update regarding recognition and management. , 1997, Current clinical topics in infectious diseases.

[44]  L. Beutin,et al.  Molecular analysis of the plasmid-encoded hemolysin of Escherichia coli O157:H7 strain EDL 933 , 1995, Infection and immunity.

[45]  R. Novick,et al.  The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus , 1998, Molecular microbiology.

[46]  D. Hooper.  Bacterial topoisomerases, anti-topoisomerases, and anti-topoisomerase resistance. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[47]  N. Craig,et al.  Tn7: a target site‐specific transposon , 1991, Molecular microbiology.

[48]  J. Hacker,et al.  A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256 , 1999, Molecular microbiology.

[49]  K. Hiramatsu,et al.  Cloning and Nucleotide Sequence Determination of the Entire mec DNA of Pre-Methicillin-Resistant Staphylococcus aureus N 315 , 1999 .

[50]  A. Tomasz,et al.  Tracking the evolutionary origin of the methicillin resistance gene: cloning and sequencing of a homologue of mecA from a methicillin susceptible strain of Staphylococcus sciuri. , 1996, Microbial drug resistance.

[51]  D. Mazel,et al.  A distinctive class of integron in the Vibrio cholerae genome. , 1998, Science.

[52]  R. Losick,et al.  Chromosomal rearrangement generating a composite gene for a developmental transcription factor. , 1989, Science.

[53]  B. Spratt,et al.  Recombinational exchanges at the capsular polysaccharide biosynthetic locus lead to frequent serotype changes among natural isolates of Streptococcus pneumoniae , 1998, Molecular microbiology.

[54]  R. Haselkorn.  Developmentally regulated gene rearrangements in prokaryotes. , 1992, Annual review of genetics.

[55]  L. Rice,et al.  Enterococcal transposon Tn5384: evolution of a composite transposon through cointegration of enterococcal and staphylococcal plasmids , 1997, Antimicrobial agents and chemotherapy.

[56]  Interaction between bacteriophage lambda and its Escherichia coli host. , 1992, Current opinion in genetics & development.

[57]  W. Haldenwang.  The sigma factors of Bacillus subtilis , 1995, Microbiological reviews.

[58]  J. Hacker,et al.  Amino acid residue Ala‐62 in the FimH fimbrial adhesin is critical for the adhesiveness of meningitis‐associated Escherichia coli to collagens , 1999, Molecular microbiology.

[59]  S. Sandler,et al.  Homologous genetic recombination: the pieces begin to fall into place. , 1994, Critical reviews in microbiology.

[60]  J. Erickson,et al.  Structural mechanisms of HIV drug resistance. , 1996, Annual review of pharmacology and toxicology.

[61]  B. Robertson,et al.  Molecular mechanisms and implications for infection of lipopolysaccharide variation in Neisseria , 1995, Molecular microbiology.

[62]  J. Musser,et al.  Antimicrobial agent resistance in mycobacteria: molecular genetic insights , 1995, Clinical microbiology reviews.

[63]  K. Dybvig,et al.  Molecular biology of mycoplasmas. , 1996, Annual review of microbiology.

[64]  D. Trees,et al.  Identification of a Staphylococcus aureus transposon (Tn4291) that carries the methicillin resistance gene(s) , 1988, Journal of bacteriology.

[65]  H. Karch,et al.  EspP, a novel extracellular serine protease of enterohaemorrhagic Escherichia coli O157:H7 cleaves human coagulation factor V , 1997, Molecular microbiology.

[66]  R. Hengge-aronis,et al.  The role of the sigma factor sigma S (KatF) in bacterial global regulation. , 1994, Annual review of microbiology.

[67]  H. Karch,et al.  KatP, a novel catalase-peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. , 1996, Microbiology.