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Editor's Pick Research Article

Novel Picornavirus Associated with Avian Keratin Disorder in Alaskan Birds

Maxine Zylberberg, Caroline Van Hemert, John P. Dumbacher, Colleen M. Handel, Tarik Tihan, Joseph L. DeRisi
David A. Relman, Editor
Maxine Zylberberg
aDepartment of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA
bCalifornia Academy of Sciences, San Francisco, California, USA
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Caroline Van Hemert
cU.S. Geological Survey, Alaska Science Center, Anchorage, Alaska, USA
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John P. Dumbacher
bCalifornia Academy of Sciences, San Francisco, California, USA
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Colleen M. Handel
cU.S. Geological Survey, Alaska Science Center, Anchorage, Alaska, USA
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Tarik Tihan
dDepartment of Pathology, University of California, San Francisco, San Francisco, California, USA
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Joseph L. DeRisi
aDepartment of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, California, USA
eHoward Hughes Medical Institute, Chevy Chase, Maryland, USA
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  • ORCID record for Joseph L. DeRisi
David A. Relman
VA Palo Alto Health Care System
Roles: Editor
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Bert Semler
University of California, Irvine
Roles: Solicited external reviewer
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Nathan Nieto
Northern Arizona University
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DOI: 10.1128/mBio.00874-16
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  • FIG 1 
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    FIG 1 

    Avian keratin disorder. (A) An unaffected BCCH. (B) BCCH 971 (beak length: 18.7 mm). (C) RBNH 929 (beak length: 29.7 mm). (B and C) Both 971 and 929 exhibit beak overgrowth characteristic of AKD.

  • FIG 2 
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    FIG 2 

    Poecivirus genome organization. (Top) Predicted genome organization. P1 (blue) represents viral structural proteins, and P2 (violet) and P3 (orange) represent nonstructural proteins. Predicted N-terminal cleavage sites are shown below the bar, and conserved picornaviral amino acid motifs are shown above it. (Middle) Number of reads from the metagenomic sequencing data set that support each base. (Bottom) Polyprotein homology between poecivirus and its closest relative, duck megrivirus, measured as the pairwise identity of a moving 15-amino-acid window.

  • FIG 3 
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    FIG 3 

    Phylogenetic tree of picornaviruses. (Top) Relationship between picornavirus polyproteins. Color indicates host taxa, with poecivirus highlighted in light red. TMEV, Theiler’s murine encephalomyelitis virus. (Bottom) Detail of boxed portion of top tree showing the relationship between poecivirus and its closest relatives; numbers indicate the percentage of bootstrap support for a given branch.

  • FIG 4 
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    FIG 4 

    Viral tropism. Relative levels of viral RNA in different tissues from poecivirus-infected BCCH individuals were measured by qRT-PCR. Levels were normalized to levels of avian cellular RNA. Buccal and cloacal swabs were only tested for BCCH 970 and 971. gi, gastrointestinal.

  • FIG 5 
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    FIG 5 

    Histopathology of AKD. (A1 and B1) Gross beak morphology of BCCH 601 (unaffected by AKD) and 498 (AKD affected; beak length is 40.3 mm), respectively. (A2 and B2) Histopathology of the beaks of BCCH 601 (A2) and 498 (B2). The black box (B2) indicates an area of cytoplasmic vacuolization of cells; the nuclei of these cells show contour irregularities and areas surrounded by a rim of clear cytoplasm, creating an “owl eye” appearance.

Tables

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  • TABLE 1 

    Description and treatment of black-capped chickadees, red-breasted nuthatches, and Northwestern crows sampled

    Species and specimenaYrAKD statusPoecivirus presentBeak length (mm)Beak appearance, histopathologyNGSbSample processing notes
    ElongatedCrossedNormal, cellular-level hyperkeratosis
    BCCH
        1602001AffectedYes9.3XYesFull Sanger sequencing of ORF
        2632001AffectedYes9.3XYes
        3942001AffectedYes9.4XYesFull Sanger sequencing of ORF
        4492002AffectedYes9.5XYesFull Sanger sequencing of ORF
        4512002AffectedYes11XYes
        4782003AffectedYes21.1XXYes
        4982004AffectedYes40.3XXYesFull Sanger sequencing of ORF
        6002006AffectedYes8.1XYes
        7382010AffectedYes8XFull Sanger sequencing of ORF
        9532014AffectedYes25.1XXStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9542014AffectedYes25.1XStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9552014AffectedYes23.1XXPoecivirus detection using virus-specific primers
        9562014AffectedYes8.7XStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9672015AffectedYes19.6XXStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9682015AffectedYes9.5XXStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9702015AffectedYes8.8XStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9712015AffectedYes18.7XXStored at 4°C overnight prior to processing for poecivirus detection using virus-specific primers
        9722015AffectedYes15.7XXPoecivirus detection using virus-specific primers
        9732015AffectedYes9.0XXPoecivirus detection using virus-specific primers
        1831995UnaffectedNo7.3Poecivirus detection using virus-specific primers
        3892001UnaffectedNo7Poecivirus detection using virus-specific primers
        3922001UnaffectedNo7.3Poecivirus detection using virus-specific primers
        4012001UnaffectedNo7.3Poecivirus detection using virus-specific primers
        4602003UnaffectedNo7.3Poecivirus detection using virus-specific primers
        4732003UnaffectedNo7.3Poecivirus detection using virus-specific primers
        5962007UnaffectedYes7Full Sanger sequencing of ORF
        6012008UnaffectedYes7.4Full Sanger sequencing of ORF
        7392010UnaffectedNo7.3Poecivirus detection using virus-specific primers
    RBNH
        121999AffectedYes12.1XXPoecivirus detection using virus-specific primers
        9292012AffectedYes29.6XXPoecivirus detection using virus-specific primers
    NOCR
        6742005AffectedYes36.3XPoecivirus detection using virus-specific primers
        8482007AffectedYes33.1XXPoecivirus detection using virus-specific primers
    • ↵a BCCH, black-capped chickadees; RBNH, red-breasted nuthatches; NOCR, northwestern crows.

    • ↵b NGS, next-generation sequencing.

Supplemental Material

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  • Table S1 

    Poecivirus-specific primers. Primer BCCHpic_1F and BCCHpic_9R, targeting the 5′ UTR and 3′ UTR, respectively, are not represented in the Sanger sequencing-validated poecivirus genome deposited in GenBank (accession number KU977108). Table S1, DOCX file, 0.01 MB.

    Copyright © 2016 Zylberberg et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Additional Files

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    Supplementary Data

    • Table st1, DOCX - Table st1, DOCX
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Novel Picornavirus Associated with Avian Keratin Disorder in Alaskan Birds
Maxine Zylberberg, Caroline Van Hemert, John P. Dumbacher, Colleen M. Handel, Tarik Tihan, Joseph L. DeRisi
mBio Jul 2016, 7 (4) e00874-16; DOI: 10.1128/mBio.00874-16

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Novel Picornavirus Associated with Avian Keratin Disorder in Alaskan Birds
Maxine Zylberberg, Caroline Van Hemert, John P. Dumbacher, Colleen M. Handel, Tarik Tihan, Joseph L. DeRisi
mBio Jul 2016, 7 (4) e00874-16; DOI: 10.1128/mBio.00874-16
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