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Title: Global Genetic Population Structure of Bacillus anthracis

Abstract

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 Amore » 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.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [4];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [3];  [1];  [5];  [1];  [4] more »;  [1];  [6] « less
+ Show Author Affiliations
  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)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)
OSTI Identifier:
1627333
Grant/Contract Number:  
AC52-06NA25396
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 2; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bacillus anthracis; single nucleotide polymorphisms; anthrax; genomics; phylogenetics; phylogeography; phylogenetic analysis; population genetics

Citation Formats

Van Ert, Matthew N., Easterday, W. Ryan, Huynh, Lynn Y., Okinaka, Richard T., Hugh-Jones, Martin E., Ravel, Jacques, Zanecki, Shaylan R., Pearson, Talima, Simonson, Tatum S., U'Ren, Jana M., Kachur, Sergey M., Leadem-Dougherty, Rebecca R., Rhoton, Shane D., Zinser, Guenevier, Farlow, Jason, Coker, Pamala R., Smith, Kimothy L., Wang, Bingxiang, Kenefic, Leo J., Fraser-Liggett, Claire M., Wagner, David M., and Keim, Paul. Global Genetic Population Structure of Bacillus anthracis. United States: N. p., 2007. Web. doi:10.1371/journal.pone.0000461.
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Van Ert, Matthew N., Easterday, W. Ryan, Huynh, Lynn Y., Okinaka, Richard T., Hugh-Jones, Martin E., Ravel, Jacques, Zanecki, Shaylan R., Pearson, Talima, Simonson, Tatum S., U'Ren, Jana M., Kachur, Sergey M., Leadem-Dougherty, Rebecca R., Rhoton, Shane D., Zinser, Guenevier, Farlow, Jason, Coker, Pamala R., Smith, Kimothy L., Wang, Bingxiang, Kenefic, Leo J., Fraser-Liggett, Claire M., Wagner, David M., & Keim, Paul. Global Genetic Population Structure of Bacillus anthracis. United States. https://doi.org/10.1371/journal.pone.0000461
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Van Ert, Matthew N., Easterday, W. Ryan, Huynh, Lynn Y., Okinaka, Richard T., Hugh-Jones, Martin E., Ravel, Jacques, Zanecki, Shaylan R., Pearson, Talima, Simonson, Tatum S., U'Ren, Jana M., Kachur, Sergey M., Leadem-Dougherty, Rebecca R., Rhoton, Shane D., Zinser, Guenevier, Farlow, Jason, Coker, Pamala R., Smith, Kimothy L., Wang, Bingxiang, Kenefic, Leo J., Fraser-Liggett, Claire M., Wagner, David M., and Keim, Paul. Wed . "Global Genetic Population Structure of Bacillus anthracis". United States. https://doi.org/10.1371/journal.pone.0000461. https://www.osti.gov/servlets/purl/1627333.
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@article{osti_1627333,
title = {Global Genetic Population Structure of Bacillus anthracis},
author = {Van Ert, Matthew N. and Easterday, W. Ryan and Huynh, Lynn Y. and Okinaka, Richard T. and Hugh-Jones, Martin E. and Ravel, Jacques and Zanecki, Shaylan R. and Pearson, Talima and Simonson, Tatum S. and U'Ren, Jana M. and Kachur, Sergey M. and Leadem-Dougherty, Rebecca R. and Rhoton, Shane D. and Zinser, Guenevier and Farlow, Jason and Coker, Pamala R. and Smith, Kimothy L. and Wang, Bingxiang and Kenefic, Leo J. and Fraser-Liggett, Claire M. and Wagner, David M. and Keim, Paul},
abstractNote = {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.},
doi = {10.1371/journal.pone.0000461},
journal = {PLoS ONE},
number = 5,
volume = 2,
place = {United States},
year = {Wed May 23 00:00:00 EDT 2007},
month = {Wed May 23 00:00:00 EDT 2007}
}
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    • PLOS Neglected Tropical Diseases, Vol. 9, Issue 4
    • DOI: 10.1371/journal.pntd.0003455

    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

    • Tourasse, Nicolas J.; Kolstø, Anne-Brit
    • Nucleic Acids Research, Vol. 36, Issue 14
    • DOI: 10.1093/nar/gkn372

    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

    • Šmajs, David; Norris, Steven J.; Weinstock, George M.
    • Infection, Genetics and Evolution, Vol. 12, Issue 2
    • DOI: 10.1016/j.meegid.2011.12.001

    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

    • Silvestri, Erin E.; Yund, Cynthia; Taft, Sarah
    • Journal of Exposure Science & Environmental Epidemiology, Vol. 27, Issue 2
    • DOI: 10.1038/jes.2016.3

    Genetic variation and linkage disequilibrium in Bacillus anthracis
    journal, November 2011

    • Zwick, Michael E.; Thomason, Maureen Kiley; Chen, Peter E.
    • Scientific Reports, Vol. 1, Issue 1
    • DOI: 10.1038/srep00169

    Coalescence modeling of intrainfection Bacillus anthracis populations allows estimation of infection parameters in wild populations
    journal, February 2020

    • Easterday, W. Ryan; Ponciano, José Miguel; Gomez, Juan Pablo
    • Proceedings of the National Academy of Sciences, Vol. 117, Issue 8
    • DOI: 10.1073/pnas.1920790117

    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

    • Tourasse, Nicolas J.; Kolstø, Anne-Brit
    • Nucleic Acids Research, Vol. 36, Issue 14
    • DOI: 10.1093/nar/gkn372

    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

    • Pullan, Steven T.; Pearson, Talima R.; Latham, Jennie
    • Microbial Genomics, Vol. 1, Issue 5
    • DOI: 10.1099/mgen.0.000039

    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

    • Antwerpen, Markus; Elschner, Mandy; Gaede, Wolfgang
    • Genome Announcements, Vol. 4, Issue 2
    • DOI: 10.1128/genomea.00219-16

    Ten Genome Sequences of Human and Livestock Isolates of Bacillus anthracis from the Country of Georgia
    journal, May 2017

    • Khmaladze, Ekaterine; Dzavashvili, Giorgi; Chanturia, Gvantsa
    • Genome Announcements, Vol. 5, Issue 19
    • DOI: 10.1128/genomea.00256-17

    Draft Genomes of Three Strains Representative of the Bacillus anthracis Diversity Found in France
    journal, August 2014

    • Girault, Guillaume; Parisot, Nicolas; Peyretaillade, Eric
    • Genome Announcements, Vol. 2, Issue 4
    • DOI: 10.1128/genomea.00736-14

    Genome Sequence of Bacillus anthracis Strain Tangail-1 from Bangladesh
    journal, August 2016

    • Rume, Farzana Islam; Antwerpen, Markus; Braun, Peter
    • Genome Announcements, Vol. 4, Issue 4
    • DOI: 10.1128/genomea.00748-16

    Genome Sequence of the Soviet/Russian Bacillus anthracis Vaccine Strain 55-VNIIVViM
    journal, December 2016

    Unexpected Relations of Historical Anthrax Strain
    journal, May 2017

    A Bacillus anthracis Genome Sequence from the Sverdlovsk 1979 Autopsy Specimens
    journal, November 2016

    Loss of Bacitracin Resistance Due to a Large Genomic Deletion among Bacillus anthracis Strains
    journal, October 2018

    An attenuated strain of Bacillus anthracis (CDC 684) has a large chromosomal inversion and altered growth kinetics
    journal, September 2011

    Indication for Co-evolution of Lactobacillus johnsonii with its hosts
    journal, January 2012

    • Buhnik-Rosenblau, Keren; Matsko-Efimov, Vera; Jung, Minju
    • BMC Microbiology, Vol. 12, Issue 1
    • DOI: 10.1186/1471-2180-12-149

    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

    • Simonson, Tatum S.; Okinaka, Richard T.; Wang, Bingxiang
    • BMC Microbiology, Vol. 9, Issue 1
    • DOI: 10.1186/1471-2180-9-71

    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

    • Satya, Ravi Vijaya; Zavaljevski, Nela; Reifman, Jaques
    • Source Code for Biology and Medicine, Vol. 6, Issue 1
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    Anthrax phylogenetic structure in Northern Italy
    journal, July 2011

    • Garofolo, Giuliano; Serrecchia, Luigina; Corrò, Michela
    • BMC Research Notes, Vol. 4, Issue 1
    • DOI: 10.1186/1756-0500-4-273

    Accurate, rapid and high-throughput detection of strain-specific polymorphisms in Bacillus anthracis and Yersinia pestis by next-generation sequencing
    journal, January 2010

    • Cummings, Craig A.; Bormann-Chung, Christina A.; Fang, Rixun
    • Investigative Genetics, Vol. 1, Issue 1
    • DOI: 10.1186/2041-2223-1-5

    Phylogenetic analysis of Bacillus anthracis strains from Western Siberia reveals a new genetic cluster in the global population of the species
    journal, September 2019

    • Pisarenko, Sergey V.; Eremenko, Eugene I.; Ryazanova, Alla G.
    • BMC Genomics, Vol. 20, Issue 1
    • DOI: 10.1186/s12864-019-6060-z

    Genetic diversity of Bacillus anthracis Ames lineage strains in China
    journal, February 2020

    Spatio-temporal patterns of an anthrax outbreak in white-tailed deer, Odocoileus virginanus, and associated genetic diversity of Bacillus anthracis
    journal, December 2015

    The reporting of a Bacillus anthracis B-clade strain in South Africa after more than 20 years
    journal, May 2018

    Phylogeography and Molecular Epidemiology of Yersinia pestis in Madagascar
    journal, September 2011

    Distribution and Molecular Evolution of Bacillus anthracis Genotypes in Namibia
    journal, March 2012

    Genetic characteristics of Bacillus anthracis isolated from northwestern China from 1990 to 2016
    journal, November 2018

    Large Direct Repeats Flank Genomic Rearrangements between a New Clinical Isolate of Francisella tularensis subsp. tularensis A1 and Schu S4
    journal, February 2010

    The Genome of a Bacillus Isolate Causing Anthrax in Chimpanzees Combines Chromosomal Properties of B. cereus with B. anthracis Virulence Plasmids
    journal, July 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

    Ecological Niche Modeling of Bacillus anthracis on Three Continents: Evidence for Genetic-Ecological Divergence?
    journal, August 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

    TaqMan Real-Time PCR Assays for Single-Nucleotide Polymorphisms Which Identify Francisella tularensis and Its Subspecies and Subpopulations
    journal, September 2014

    Whole Genome-Sequencing and Phylogenetic Analysis of a Historical Collection of Bacillus anthracis Strains from Danish Cattle
    journal, August 2015

    Microevolution of Anthrax from a Young Ancestor (M.A.Y.A.) Suggests a Soil-Borne Life Cycle of Bacillus anthracis
    journal, August 2015

    Investigation of Anthrax Cases in North-East China, 2010-2014
    journal, August 2015

    Comparison of French and Worldwide Bacillus anthracis Strains Favors a Recent, Post-Columbian Origin of the Predominant North-American Clade
    journal, February 2016

    Phylogenetic Characteristics of Anthrax Outbreaks in Liaoning Province, China, 2001-2015
    journal, June 2016

    Spatio-temporal epidemiology of anthrax in Hippopotamus amphibious in Queen Elizabeth Protected Area, Uganda
    journal, November 2018

    Genetic characterization of Bacillus anthracis strains circulating in Italy from 1972 to 2018
    journal, January 2020

    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

    • Okinaka, Richard T.; Henrie, Melinda; Hill, Karen K.
    • Emerging Infectious Diseases, Vol. 14, Issue 4
    • DOI: 10.3201/eid1404.070984

    Texas Isolates Closely Related to Bacillus anthracis Ames
    journal, September 2008

    • Kenefic, Leo J.; Pearson, Talima; Okinaka, Richard T.
    • Emerging Infectious Diseases, Vol. 14, Issue 9
    • DOI: 10.3201/eid1409.080076

    Molecular Epidemiologic Investigation of an Anthrax Outbreak among Heroin Users, Europe
    journal, August 2012

    • Price, Erin P.; Seymour, Meagan L.; Sarovich, Derek S.
    • Emerging Infectious Diseases, Vol. 18, Issue 8
    • DOI: 10.3201/eid1808.111343

    Injectional Anthrax in Heroin Users, Europe, 2000–2012
    journal, February 2014

    • Hanczaruk, Matthias; Reischl, Udo; Holzmann, Thomas
    • Emerging Infectious Diseases, Vol. 20, Issue 2
    • DOI: 10.3201/eid2002.120921

    Linking Geospatial and Laboratory Sciences to Define Mechanisms behind Landscape Level Drivers of Anthrax Outbreaks
    journal, October 2019

    • Norris, Michael H.; Blackburn, Jason K.
    • International Journal of Environmental Research and Public Health, Vol. 16, Issue 19
    • DOI: 10.3390/ijerph16193747

    Evaluation of in vitro antimicrobial susceptibility of Bacillus anthracis strains isolated during anthrax outbreaks in Italy from 1984 to 2017
    journal, January 2019

    • Manzulli, Viviana; Fasanella, Antonio; Parisi, Antonio
    • Journal of Veterinary Science, Vol. 20, Issue 1
    • DOI: 10.4142/jvs.2019.20.1.58

    Development of a temperature-switch PCR-based SNP typing method for Mycobacterium ulcerans
    text, January 2012

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