Pathogenic Bacillus anthracis in the progressive gene losses and gains in adaptive evolution

BackgroundSequence mutations represent a driving force of adaptive evolution in bacterial pathogens. It is especially evident in reductive genome evolution where bacteria underwent lifestyles shifting from a free-living to a strictly intracellular or host-depending life. It resulted in loss-of-function mutations and/or the acquisition of virulence gene clusters. Bacillus anthracis shares a common soil bacterial ancestor with its closely related bacillus species but is the only obligate, causative agent of inhalation anthrax within the genus Bacillus. The anthrax-causing Bacillus anthracis experienced the similar lifestyle changes. We thus hypothesized that the bacterial pathogen would follow a compatible evolution path.ResultsIn this study, a cluster-based evolution scheme was devised to analyze genes that are gained by or lost from B. anthracis. The study detected gene losses/gains at two separate evolutionary stages. The stage I is when B. anthracis and its sister species within the Bacillus cereus group diverged from other species in genus Bacillus. The stage II is when B. anthracis differentiated from its two closest relatives: B. cereus and B. thuringiensis. Many genes gained at these stages are homologues of known pathogenic factors such those for internalin, B. anthracis-specific toxins and large groups of surface proteins and lipoproteins.ConclusionThe analysis presented here allowed us to portray a progressive evolutionary process during the lifestyle shift of B. anthracis, thus providing new insights into how B. anthracis had evolved and bore a promise of finding drug and vaccine targets for this strategically important pathogen.

[1]  S. Salzberg,et al.  The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria , 2003, Nature.

[2]  Jay E Gee,et al.  Molecular approaches to identify and differentiate Bacillus anthracis from phenotypically similar Bacillus species isolates , 2006, BMC Microbiology.

[3]  Edward A Graviss,et al.  Genome-Wide Analysis of Group A Streptococci Reveals a Mutation That Modulates Global Phenotype and Disease Specificity , 2006, PLoS pathogens.

[4]  Lynne A. Goodwin,et al.  Pathogenomic Sequence Analysis of Bacillus cereus and Bacillus thuringiensis Isolates Closely Related to Bacillus anthracis , 2006, Journal of bacteriology.

[5]  Eduardo P C Rocha,et al.  Reconstructing the ancestor of Mycobacterium leprae: the dynamics of gene loss and genome reduction. , 2007, Genome research.

[6]  R. Overbeek,et al.  The use of gene clusters to infer functional coupling. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N. Moran,et al.  Deletional bias and the evolution of bacterial genomes. , 2001, Trends in genetics : TIG.

[8]  S. Abbott,et al.  Virulence markers of mesophilic aeromonads: association of the autoagglutination phenomenon with mouse pathogenicity and the presence of a peripheral cell-associated layer , 1987, Infection and immunity.

[9]  S Miyano,et al.  Open source clustering software. , 2004, Bioinformatics.

[10]  M. Uyttendaele,et al.  Differential inlA and inlB Expression and Interaction with Human Intestinal and Liver Cells by Listeria monocytogenes Strains of Different Origins , 2006, Applied and Environmental Microbiology.

[11]  K. Weaver,et al.  Molecular Characterization of Mycoplasma arthritidis Membrane Lipoprotein MAA1 , 2000, Infection and Immunity.

[12]  T. Raffin,et al.  Inhalational anthrax: epidemiology, diagnosis, and management. , 1999, Chest.

[13]  D. Knowles,et al.  Distinctly different msp2 pseudogene repertoires in Anaplasma marginale strains that are capable of superinfection. , 2005, Gene.

[14]  David A Rasko,et al.  The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. , 2004, Nucleic acids research.

[15]  D. Garmyn,et al.  Truncated Internalin A and Asymptomatic Listeria monocytogenes Carriage: In Vivo Investigation by Allelic Exchange , 2005, Infection and Immunity.

[16]  A. Maurelli Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. , 2007, FEMS microbiology letters.

[17]  C. Nielsen-Leroux,et al.  Identification of Bacillus cereus internalin and other candidate virulence genes specifically induced during oral infection in insects , 2006, Molecular microbiology.

[18]  A. Maurelli,et al.  The Mxi-Spa Type III Secretory Pathway ofShigella flexneri Requires an Outer Membrane Lipoprotein, MxiM, for Invasin Translocation , 1999, Infection and Immunity.

[19]  J. Wernegreen,et al.  Genome evolution in bacterial endosymbionts of insects , 2002, Nature Reviews Genetics.

[20]  J Hacker,et al.  Evolution of microbial pathogens. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  M. Mock,et al.  Germination of Bacillus anthracis spores within alveolar macrophages , 1999, Molecular microbiology.

[22]  B. Wilson,et al.  Is the evolution of bacterial pathogens an out-of-body experience? , 2003, Trends in microbiology.

[23]  Michal J. Nagiec,et al.  Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[24]  B. Barrell,et al.  The Chlamydophila abortus genome sequence reveals an array of variable proteins that contribute to interspecies variation. , 2005, Genome research.

[25]  Alok J. Saldanha,et al.  Java Treeview - extensible visualization of microarray data , 2004, Bioinform..

[26]  P. Piveteau,et al.  Expression of Truncated Internalin A Is Involved in Impaired Internalization of Some Listeria monocytogenes Isolates Carried Asymptomatically by Humans , 2003, Infection and Immunity.

[27]  J. Parkhill,et al.  Evolutionary strategies of human pathogens. , 2003, Cold Spring Harbor symposia on quantitative biology.

[28]  J. Côté,et al.  Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3' end 16S rDNA and 5' end 16S-23S ITS nucleotide sequences. , 2003, International journal of systematic and evolutionary microbiology.

[29]  P. Cossart Molecular and cellular basis of the infection by Listeria monocytogenes: an overview. , 2002, International journal of medical microbiology : IJMM.

[30]  M. Mock,et al.  Fate of germinated Bacillus anthracis spores in primary murine macrophages , 2001, Molecular microbiology.

[31]  C. Kurland,et al.  Reductive evolution of resident genomes. , 1998, Trends in microbiology.

[32]  M. Kostrzynska,et al.  Antigenic diversity of the S-layer proteins from pathogenic strains of Aeromonas hydrophila and Aeromonas veronii biotype sobria , 1992, Journal of bacteriology.

[33]  M. Popoff,et al.  Nucleotide sequence of iagA and iagB genes involved in invasion of HeLa cells by Salmonella enterica subsp. enterica ser. Typhi. , 1995, Research in microbiology.

[34]  G. Sternbach The history of anthrax. , 2003, The Journal of emergency medicine.

[35]  P. Berche,et al.  OppA of Listeria monocytogenes, an Oligopeptide-Binding Protein Required for Bacterial Growth at Low Temperature and Involved in Intracellular Survival , 2000, Infection and Immunity.

[36]  S. Ehrlich,et al.  Multiple-Locus Sequence Typing Analysis of Bacillus cereus and Bacillus thuringiensis Reveals Separate Clustering and a Distinct Population Structure of Psychrotrophic Strains , 2006, Applied and Environmental Microbiology.

[37]  Erin Beck,et al.  The comprehensive microbial resource , 2000, Nucleic Acids Res..

[38]  R. R. Granados,et al.  Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. , 1996, Journal of invertebrate pathology.

[39]  P. E. Granum,et al.  Genetic and functional analysis of the cytK family of genes in Bacillus cereus. , 2004, Microbiology.