skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Global Genetic Population Structure of Bacillus anthracis

Journal Article · · PLoS ONE
 [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [1];  [5];  [1];  [4] more »;  [1];  [6] « less
  1. Northern Arizona University, Flagstaff, AZ (United States)
  2. Northern Arizona University, Flagstaff, AZ (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
  3. Louisiana State University, Baton Rouge, LA (United States)
  4. The Institute for Genomic Research, Rockville, MD (United States)
  5. Lanzhou Institute of Biological Products, Lanzhou (China)
  6. Northern Arizona University, Flagstaff, AZ (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Translational Genomics Research Institute, Phoenix, AZ (United States)

Anthrax, caused by the bacterium Bacillus anthracis, is a disease of historical and current importance that is found throughout the world. The basis of its historical transmission is anecdotal and its true global population structure has remained largely cryptic. Seven diverse B. anthracis strains were whole-genome sequenced to identify rare single nucleotide polymorphisms (SNPs), followed by phylogenetic reconstruction of these characters onto an evolutionary model. This analysis identified SNPs that define the major clonal lineages within the species. These SNPs, in concert with 15 variable number tandem repeat (VNTR) markers, were used to subtype a collection of 1,033 B. anthracis isolates from 42 countries to create an extensive genotype data set. These analyses subdivided the isolates into three previously recognized major lineages (A, B, and C), with further subdivision into 12 clonal sub-lineages or sub-groups and, finally, 221 unique MLVA15 genotypes. This rare genomic variation was used to document the evolutionary progression of B. anthracis and to establish global patterns of diversity. Isolates in the A lineage are widely dispersed globally, whereas the B and C lineages occur on more restricted spatial scales. Molecular clock models based upon genome-wide synonymous substitutions indicate there was a massive radiation of the A lineage that occurred in the mid-Holocene (3,064–6,127 ybp). On more recent temporal scales, the global population structure of B. anthracis reflects colonial-era importation of specific genotypes from the Old World into the New World, as well as the repeated industrial importation of diverse genotypes into developed countries via spore-contaminated animal products. These findings indicate humans have played an important role in the evolution of anthrax by increasing the proliferation and dispersal of this now global disease. Finally, the value of global genotypic analysis for investigating bioterrorist-mediated outbreaks of anthrax is demonstrated.

Research Organization:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
Grant/Contract Number:
AC52-06NA25396
OSTI ID:
1627333
Journal Information:
PLoS ONE, Vol. 2, Issue 5; ISSN 1932-6203
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (39)

Identifying Sources of Human Exposure to Plague journal February 2005
Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from whole-genome sequencing journal September 2004
Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis journal May 2002
Anthrax and Bone-Meal Fertiliser journal July 1958
Ecology of Anthrax journal June 1971
Mitochondrial diversity and the origins of African and European cattle. journal May 1996
Epidemiology of a Small Outbreak of Anthrax journal May 1951
MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment journal January 2004
Identifying Sources of Human Exposure to Plague journal April 2005
A haplotype map of the human genome journal March 2003
Anthrax, but Not Bacillus anthracis? journal January 2006
The incompatibility between the PlcR- and AtxA-controlled regulons may have selected a nonsense mutation in Bacillus anthracis: The PlcR-controlled regulon in B. anthracis journal December 2001
Rates of Spontaneous Mutation journal April 1998
Evolution, consequences and future of plant and animal domestication journal August 2002
Molecular Subtyping of Bacillus anthracis and the 2001 Bioterrorism-Associated Anthrax Outbreak, United States journal October 2002
Ecological constraints on diversification in a model adaptive radiation journal October 2004
Characterization of a Bacillus anthracis Isolate Causing a Rare Case of Fatal Anthrax in a 2-Year-Old Boy from Hong Kong journal April 2005
Comparative Genome Sequencing for Discovery of Novel Polymorphisms in Bacillus anthracis journal May 2002
Intriguing diversity of Bacillus anthracis in eastern Poland – the molecular echoes of the past outbreaks journal October 2004
A review of anthrax in Canada and implications for research on the disease in northern bison journal August 1999
Multiple-Locus Variable-Number Tandem Repeat Analysis Reveals Genetic Relationships within Bacillus anthracis journal December 2000
The Distribution of Rates of Spontaneous Mutation over Viruses, Prokaryotes, and Eukaryotes journal May 1999
In Vivo Growth and Distribution of Anthrax Bacilli in Resistant, Susceptible, and Immunized Hosts journal January 1967
Strain-Specific Single-Nucleotide Polymorphism Assays for the Bacillus anthracis Ames Strain journal November 2006
Methicillin-resistant Staphylococcus aureus genotyping using a small set of polymorphisms journal January 2006
High-Throughput Single Nucleotide Polymorphism Genotyping by Fluorescent 5′ Exonuclease Assay journal September 1999
Anthrax molecular epidemiology and forensics: using the appropriate marker for different evolutionary scales journal September 2004
Genomics: Anthrax and the art of war (against ascertainment bias) journal January 2005
Anthrax and Bone-Meal Fertiliser journal March 1955
Molecular Analysis of Rifampin Resistance in Bacillus anthracis and Bacillus cereus journal February 2002
Multiple-Locus Variable-Number Tandem Repeat Analysis Reveals Genetic Relationships within Bacillus anthracis journal May 2000
Distinct Mutations in PlcR Explain Why Some Strains of the Bacillus cereus Group Are Nonhemolytic journal June 2004
Antibiotic Susceptibility and Molecular Diversity of Bacillus anthracis Strains in Chad: Detection of a New Phylogenetic Subgroup journal September 2006
Bacillus anthracis Diversity in Kruger National Park journal January 2000
Molecular Investigation of the Aum Shinrikyo Anthrax Release in Kameido, Japan journal December 2001
Diversity among French Bacillus anthracis Isolates journal December 2002
Use of Single Nucleotide Polymorphisms in the plcR Gene for Specific Identification of Bacillus anthracis journal April 2005
Molecular Diversity of Bacillus anthracis in Italy journal July 2005
The Milroy Lectures ON INDUSTRIAL ANTHRAX: Delivered before the Royal College of Physicians of London journal March 1905

Cited By (107)

Melt Analysis of Mismatch Amplification Mutation Assays (Melt-MAMA): A Functional Study of a Cost-Effective SNP Genotyping Assay in Bacterial Models journal March 2012
Phylogenetic Characteristics of Anthrax Outbreaks in Liaoning Province, China, 2001-2015 journal June 2016
Microevolution of Anthrax from a Young Ancestor (M.A.Y.A.) Suggests a Soil-Borne Life Cycle of Bacillus anthracis journal August 2015
Phylogenetic Placement of Isolates Within the Trans-Eurasian Clade A.Br.008/009 of Bacillus anthracis journal December 2019
Genetic source tracking of an anthrax outbreak in Shaanxi province, China journal January 2017
A classification framework for Bacillus anthracis defined by global genomic structure journal January 2020
Nucleotide polymorphism assay for the identification of west African group Bacillus anthracis: a lineage lacking anthrose journal January 2020
Genotyping of French Bacillus anthracis Strains Based on 31-Loci Multi Locus VNTR Analysis: Epidemiology, Marker Evaluation, and Update of the Internet Genotype Database journal June 2014
Application of loop mediated isothermal dna amplification to reveal and identify Bacillus anthracis journal January 2017
A classification framework for Bacillus anthracis defined by global genomic structure posted_content January 2019
Bacillus cereus Biovar Anthracis Causing Anthrax in Sub-Saharan Africa—Chromosomal Monophyly and Broad Geographic Distribution journal September 2016
Distribution and Molecular Evolution of Bacillus anthracis Genotypes in Namibia journal March 2012
Bacillus anthracis comparative genome analysis in support of the Amerithrax investigation journal March 2011
Laboratory strains of Bacillus anthracis lose their ability to rapidly grow and sporulate compared to wildlife outbreak strains journal January 2020
The identification of novel single nucleotide polymorphisms to assist in mapping the spread of Bacillus anthracis across the Southern Caucasus journal July 2018
CanSNPer: a hierarchical genotype classifier of clonal pathogens journal February 2014
Biological and Molecular-Genetic Properties of Bacillus anthracis strains Isolated in Siberia and Far East Regions (1959–2013) journal October 2018
Linking Geospatial and Laboratory Sciences to Define Mechanisms behind Landscape Level Drivers of Anthrax Outbreaks journal October 2019
Predominant Effect of Host Genetics on Levels of Lactobacillus johnsonii Bacteria in the Mouse Gut journal July 2011
Spatio-temporal patterns of an anthrax outbreak in white-tailed deer, Odocoileus virginanus, and associated genetic diversity of Bacillus anthracis journal December 2015
Historical Distribution and Molecular Diversity of Bacillus anthracis , Kazakhstan journal May 2010
Analysis of a newly discovered antigen of Bacillus cereus biovar anthracis for its suitability in specific serological antibody testing journal October 2018
Development of a Temperature-Switch PCR-Based SNP Typing Method for Mycobacterium ulcerans journal November 2012
Bovine Bacillus anthracis in Cameroon journal August 2011
Injectional Anthrax in Heroin Users, Europe, 2000–2012 journal February 2014
Genotyping of Genetically Monomorphic Bacteria: DNA Sequencing in Mycobacterium tuberculosis Highlights the Limitations of Current Methodologies journal November 2009
Genotyping and phylogenetic location of one clinical isolate of Bacillus anthracis isolated from a human in Russia journal July 2019
Indication for Co-evolution of Lactobacillus johnsonii with its hosts journal January 2012
Bacillus anthracis Diversity and Geographic Potential across Nigeria, Cameroon and Chad: Further Support of a Novel West African Lineage journal August 2015
A Bacillus anthracis Genome Sequence from the Sverdlovsk 1979 Autopsy Specimens journal November 2016
Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish journal January 2012
Loss of Bacitracin Resistance Due to a Large Genomic Deletion among Bacillus anthracis Strains journal October 2018
Bacillus anthracis Diversity and Geographic Potential across Nigeria, Cameroon and Chad: Further Support of a Novel West African Lineage. text January 2015
Texas Isolates Closely Related to Bacillus anthracis Ames journal September 2008
Spores and soil from six sides: interdisciplinarity and the environmental biology of anthrax ( Bacillus anthracis ): The environmental biology of Bacillus anthracis journal May 2018
Whole Genome Sequencing for Studying Bacillus anthracis from an Outbreak in the Abruzzo Region of Italy journal January 2020
Development of a temperature-switch PCR-based SNP typing method for Mycobacterium ulcerans text January 2012
Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia journal May 2019
Whole Genome-Sequencing and Phylogenetic Analysis of a Historical Collection of Bacillus anthracis Strains from Danish Cattle journal August 2015
The Secret Life of the Anthrax Agent Bacillus anthracis: Bacteriophage-Mediated Ecological Adaptations journal August 2009
Use of Red Beet (Beta vulgaris L.) for Antimicrobial Applications—a Critical Review journal July 2017
Anthrax outbreak in a Swedish beef cattle herd - 1st case in 27 years: Case report journal February 2010
Identification and Validation of Specific Markers of Bacillus anthracis Spores by Proteomics and Genomics Approaches journal March 2014
Genotype diversity of Bacillus anthracis strains isolated from the Caucasus region journal April 2012
Quantitative Determination of Lethal Toxin Proteins in Culture Supernatant of Human Live Anthrax Vaccine Bacillus anthracis A16R journal February 2016
Phylogenetic analysis of Bacillus anthracis strains from Western Siberia reveals a new genetic cluster in the global population of the species journal September 2019
Investigation of Anthrax Cases in North-East China, 2010-2014 journal August 2015
Genetic characteristics of Bacillus anthracis isolated from northwestern China from 1990 to 2016 journal November 2018
Investigation and source-tracing of an anthrax outbreak in Gansu Province, China journal August 2018
Comparison of spatiotemporal patterns of historic natural Anthrax outbreaks in Minnesota and Kazakhstan journal May 2019
Insights from Bacillus anthracis strains isolated from permafrost in the tundra zone of Russia posted_content January 2018
Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases journal October 2009
Lineage-specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group journal April 2018
High-throughput sequencing of Bacillus anthracis in France: investigating genome diversity and population structure using whole-genome SNP discovery journal January 2014
A proposal for a portal to make earth’s microbial diversity easily accessible and searchable journal March 2017
Comparison of French and Worldwide Bacillus anthracis Strains Favors a Recent, Post-Columbian Origin of the Predominant North-American Clade journal February 2016
Genomic and SNP Analyses Demonstrate a Distant Separation of the Hospital and Community-Associated Clades of Enterococcus faecium journal January 2012
Injectional Anthrax in Heroin Users, Europe, 2000–2012 journal February 2014
Genotyping and phylogenetic placement of Bacillus anthracis isolates from Finland, a country with rare anthrax cases journal September 2018
The reporting of a Bacillus anthracis B-clade strain in South Africa after more than 20 years journal May 2018
A Bacillus anthracis Genome Sequence from the Sverdlovsk 1979 Autopsy Specimens posted_content August 2016
The Genome of a Bacillus Isolate Causing Anthrax in Chimpanzees Combines Chromosomal Properties of B. cereus with B. anthracis Virulence Plasmids journal July 2010
Ecological Niche Modeling of Bacillus anthracis on Three Continents: Evidence for Genetic-Ecological Divergence? journal August 2013
Genetic characterization of Bacillus anthracis strains circulating in Italy from 1972 to 2018 journal January 2020
Genetic Diversity among Bacillus anthracis Soil Isolates at Fine Geographic Scales journal September 2012
Correction: Comparison of French and Worldwide Bacillus anthracis Strains Favors a Recent, Post-Columbian Origin of the Predominant North-American Clade journal June 2017
Capsules, Toxins and AtxA as Virulence Factors of Emerging Bacillus cereus Biovar anthracis journal April 2015
Survey of group I and group II introns in 29 sequenced genomes of the Bacillus cereus group: insights into their spread and evolution journal June 2008
Molecular Genotyping of Microbes by Multilocus PCR and Mass Spectrometry: A New Tool for Hospital Infection Control and Public Health Surveillance book January 2009
Whole Genome Analysis of Injectional Anthrax Identifies Two Disease Clusters Spanning More Than 13 Years journal November 2015
Genetic diversity in Treponema pallidum: Implications for pathogenesis, evolution and molecular diagnostics of syphilis and yaws journal March 2012
Optimization of a sample processing protocol for recovery of Bacillus anthracis spores from soil journal November 2016
Whole genome SNP analysis of bovine B. anthracis strains from Switzerland reflects strict regional separation of Simmental and Swiss Brown breeds in the past journal November 2016
Considerations for estimating microbial environmental data concentrations collected from a field setting journal February 2016
Genetic variation and linkage disequilibrium in Bacillus anthracis journal November 2011
Coalescence modeling of intrainfection Bacillus anthracis populations allows estimation of infection parameters in wild populations journal February 2020
Whole-genome sequencing investigation of animal-skin-drum-associated UK anthrax cases reveals evidence of mixed populations and relatedness to a US case journal November 2015
Draft Genome Sequences of Two Bulgarian Bacillus anthracis Strains journal May 2013
Genome Sequence of Bacillus anthracis Strain Stendal, Isolated from an Anthrax Outbreak in Cattle in Germany journal April 2016
Ten Genome Sequences of Human and Livestock Isolates of Bacillus anthracis from the Country of Georgia journal May 2017
Draft Genomes of Three Strains Representative of the Bacillus anthracis Diversity Found in France journal August 2014
Genome Sequence of Bacillus anthracis Strain Tangail-1 from Bangladesh journal August 2016
Genome Sequence of the Soviet/Russian Bacillus anthracis Vaccine Strain 55-VNIIVViM journal December 2016
Unexpected Relations of Historical Anthrax Strain journal May 2017
An attenuated strain of Bacillus anthracis (CDC 684) has a large chromosomal inversion and altered growth kinetics journal September 2011
Assignment of Streptococcus agalactiae isolates to clonal complexes using a small set of single nucleotide polymorphisms journal August 2008
Bacillus anthracis in China and its relationship to worldwide lineages journal January 2009
Ecological Niche Modelling of the Bacillus anthracis A1.a sub-lineage in Kazakhstan journal December 2011
SNIT: SNP identification for strain typing journal September 2011
Anthrax phylogenetic structure in Northern Italy journal July 2011
Accurate, rapid and high-throughput detection of strain-specific polymorphisms in Bacillus anthracis and Yersinia pestis by next-generation sequencing journal January 2010
Genetic diversity of Bacillus anthracis Ames lineage strains in China journal February 2020
Phylogeography and Molecular Epidemiology of Yersinia pestis in Madagascar journal September 2011
Large Direct Repeats Flank Genomic Rearrangements between a New Clinical Isolate of Francisella tularensis subsp. tularensis A1 and Schu S4 journal February 2010
Pseudomonas syringae pv. actinidiae (PSA) Isolates from Recent Bacterial Canker of Kiwifruit Outbreaks Belong to the Same Genetic Lineage journal May 2012
Use of a Bacteriophage Lysin to Identify a Novel Target for Antimicrobial Development journal April 2013
Constraints on Genome Dynamics Revealed from Gene Distribution among the Ralstonia solanacearum Species journal May 2013
Four Genotyping Schemes for Phylogenetic Analysis of Pseudomonas aeruginosa: Comparison of Their Congruence with Multi-Locus Sequence Typing journal December 2013
Eight New Genomes and Synthetic Controls Increase the Accessibility of Rapid Melt-MAMA SNP Typing of Coxiella burnetii journal January 2014
Microevolution during an Anthrax Outbreak Leading to Clonal Heterogeneity and Penicillin Resistance journal February 2014
A System to Automatically Classify and Name Any Individual Genome-Sequenced Organism Independently of Current Biological Classification and Nomenclature journal February 2014
TaqMan Real-Time PCR Assays for Single-Nucleotide Polymorphisms Which Identify Francisella tularensis and Its Subspecies and Subpopulations journal September 2014
Spatio-temporal epidemiology of anthrax in Hippopotamus amphibious in Queen Elizabeth Protected Area, Uganda journal November 2018
The Plant Pathogen Pseudomonas syringae pv. tomato Is Genetically Monomorphic and under Strong Selection to Evade Tomato Immunity journal August 2011
Single Nucleotide Polymorphism Typing ofBacillus anthracisfrom Sverdlovsk Tissue journal April 2008
Molecular Epidemiologic Investigation of an Anthrax Outbreak among Heroin Users, Europe journal August 2012
Evaluation of in vitro antimicrobial susceptibility of Bacillus anthracis strains isolated during anthrax outbreaks in Italy from 1984 to 2017 journal January 2019