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Public and Environmental Health Microbiology

Burkholderia humptydooensis sp. nov., a New Species Related to Burkholderia thailandensis and the Fifth Member of the Burkholderia pseudomallei Complex

Apichai Tuanyok, Mark Mayo, Holger Scholz, Carina M. Hall, Christopher J. Allender, Mirjam Kaestli, Jennifer Ginther, Senanu Spring-Pearson, Molly C. Bollig, Joshua K. Stone, Erik W. Settles, Joseph D. Busch, Lindsay Sidak-Loftis, Jason W. Sahl, Astrid Thomas, Lisa Kreutzer, Enrico Georgi, Jay E. Gee, Richard A. Bowen, Jason T. Ladner, Sean Lovett, Galina Koroleva, Gustavo Palacios, David M. Wagner, Bart J. Currie, Paul Keim
Donald W. Schaffner, Editor
Apichai Tuanyok
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Mark Mayo
bMenzies School of Health Research, Charles Darwin University, and Northern Territory Medical Program, Royal Darwin Hospital, Darwin, Northern Territory, Australia
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Holger Scholz
cBundeswehr Institute of Microbiology, Munich, Germany
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Carina M. Hall
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Christopher J. Allender
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Mirjam Kaestli
bMenzies School of Health Research, Charles Darwin University, and Northern Territory Medical Program, Royal Darwin Hospital, Darwin, Northern Territory, Australia
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Jennifer Ginther
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Senanu Spring-Pearson
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Molly C. Bollig
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Joshua K. Stone
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Erik W. Settles
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Joseph D. Busch
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Lindsay Sidak-Loftis
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Jason W. Sahl
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Astrid Thomas
cBundeswehr Institute of Microbiology, Munich, Germany
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Lisa Kreutzer
cBundeswehr Institute of Microbiology, Munich, Germany
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Enrico Georgi
cBundeswehr Institute of Microbiology, Munich, Germany
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Jay E. Gee
dBacterial Special Pathogens Branch, Division of High-Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
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Richard A. Bowen
eDepartment of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA
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Jason T. Ladner
fCenter for Genome Sciences, USAMRIID, Fort Detrick, Maryland, USA
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Sean Lovett
fCenter for Genome Sciences, USAMRIID, Fort Detrick, Maryland, USA
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Galina Koroleva
fCenter for Genome Sciences, USAMRIID, Fort Detrick, Maryland, USA
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Gustavo Palacios
fCenter for Genome Sciences, USAMRIID, Fort Detrick, Maryland, USA
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David M. Wagner
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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Bart J. Currie
bMenzies School of Health Research, Charles Darwin University, and Northern Territory Medical Program, Royal Darwin Hospital, Darwin, Northern Territory, Australia
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Paul Keim
aDepartment of Biological Sciences and The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
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  • ORCID record for Paul Keim
Donald W. Schaffner
Rutgers, The State University of New Jersey
Roles: Editor
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DOI: 10.1128/AEM.02802-16
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  • FIG 1
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    FIG 1

    Colony morphology of B. humptydooensis sp. nov. MSMB43T. Cultures were grown on Ashdown's agar (a) or on Standard I nutrient agar (b).

  • FIG 2
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    FIG 2

    Core genome phylogeny of B. humptydooensis sp. nov. SNPs from the comparison of four B. humptydooensis sp. nov. genomes and representatives of the other closely related species were used to reconstruct the phylogenetic relationships. Genomes from this study are shown in bold and assembly numbers are provided inside parentheses. Numbers at nodes indicate bootstrap support values. Collapsed nodes are shown in gray.

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  • TABLE 1

    Phenotypic characteristics of B. humptydooensis sp. nov. and closely related species within the B. pseudomallei group

    Biochemical reactionCharacteristic (compound present in medium or assimilated by strain)
    B. pseudomallei K96243aB. thailandensis E264TB. humptydooensis sp. nov. MSMB43TB. humptydooensis sp. nov. MSMB121B. humptydooensis sp. nov. MSMB122
    Tryptophan+−−−−
    Arginine+−+−−
    Esculin−++++
    PNPG−−−−+
    Arabinose assimilation−++++
    Maltose assimilation−+−−−
    • ↵a Data for B. pseudomallei K96243 were obtained from Wuthiekanun et al. (29).

  • TABLE 2

    Summary of MICs determined in triplicate by the broth microdilution method

    Antimicrobial substanceMIC (mg/liter)
    MSMB43TMSMB121MSMB122
    Amoxicillin-clavulanic acida32/1632/1632/16
    Ceftazidime424
    Imipenem0.50.50.5
    Rifampin>8>88
    Chloramphenicol844
    Trimethoprim-sulfamethoxazole0.5/9.5≤0.25/4.75≤0.25/4.75
    Streptomycin>32>32>32
    Gentamicin3232>32
    Doxycycline111
    Tigecycline244
    Ciprofloxacin0.511
    Levofloxacin0.511
    • ↵a Resistance was observed, based upon the CLSI breakpoints of B. pseudomallei.

  • TABLE 3

    Whole-genome dataa for B. pseudomallei group organisms

    Species and strainGC content (%)Genome size (Mb)No. of CDSc
    B. humptydooensis sp. nov. MSMB43T67.17.3b6,324
    B. humptydooensis sp. nov. MSMB12167.56.75,795
    B. humptydooensis sp. nov. MSMB12267.56.85,845
    B. thailandensis E264T67.66.75,652
    B. oklahomensis C6786T66.97.16,097
    B. pseudomallei K9624368.17.25,948
    B. mallei ATCC 23344T68.55.85,006
    • ↵a Two chromosomes are present in all genomes shown.

    • ↵b One plasmid present.

    • ↵c CDS, coding DNA sequences.

  • TABLE 4

    GGDC and ANI values for whole-genome sequence similarities

    TABLE 4
    • a Genome-to-genome distance calculations (with confidence intervals) are shown in the bottom left half of the matrix (below the line of identity, i.e., the line formed by blank cells for comparisons of strains with themselves); average nucleotide identities are shown in the top right half of the matrix. Values in shaded boxes represent values above the similarity threshold that defines members of the same species.

Additional Files

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    • Supplemental file 1 -

      Detailed methods: MALDI-TOF and FAME profile analysis; dendrogram demonstrating strain relatedness revealed by MALDI-TOF analysis (Fig. S1); dendrogram demonstrating the relatedness of fatty acid compositions in B. humptydooensis sp. nov. and closely related species (Fig. S2); 16S maximum-likelihood phylogeny using both copies of the 16S rRNA gene from each B. humptydooensis sp. nov. strain (Fig. S3); maximum-likelihood phylogeny of the recA sequence using 193 sequences (Fig. S4).

      PDF, 452K

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Burkholderia humptydooensis sp. nov., a New Species Related to Burkholderia thailandensis and the Fifth Member of the Burkholderia pseudomallei Complex
Apichai Tuanyok, Mark Mayo, Holger Scholz, Carina M. Hall, Christopher J. Allender, Mirjam Kaestli, Jennifer Ginther, Senanu Spring-Pearson, Molly C. Bollig, Joshua K. Stone, Erik W. Settles, Joseph D. Busch, Lindsay Sidak-Loftis, Jason W. Sahl, Astrid Thomas, Lisa Kreutzer, Enrico Georgi, Jay E. Gee, Richard A. Bowen, Jason T. Ladner, Sean Lovett, Galina Koroleva, Gustavo Palacios, David M. Wagner, Bart J. Currie, Paul Keim
Applied and Environmental Microbiology Feb 2017, 83 (5) e02802-16; DOI: 10.1128/AEM.02802-16

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Burkholderia humptydooensis sp. nov., a New Species Related to Burkholderia thailandensis and the Fifth Member of the Burkholderia pseudomallei Complex
Apichai Tuanyok, Mark Mayo, Holger Scholz, Carina M. Hall, Christopher J. Allender, Mirjam Kaestli, Jennifer Ginther, Senanu Spring-Pearson, Molly C. Bollig, Joshua K. Stone, Erik W. Settles, Joseph D. Busch, Lindsay Sidak-Loftis, Jason W. Sahl, Astrid Thomas, Lisa Kreutzer, Enrico Georgi, Jay E. Gee, Richard A. Bowen, Jason T. Ladner, Sean Lovett, Galina Koroleva, Gustavo Palacios, David M. Wagner, Bart J. Currie, Paul Keim
Applied and Environmental Microbiology Feb 2017, 83 (5) e02802-16; DOI: 10.1128/AEM.02802-16
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

Burkholderia
Burkholderia pseudomallei
phylogeny
Burkholderia humptydooensis sp. nov.
Burkholderia pseudomallei complex
MSMB43T

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