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Research Article | Applied and Environmental Science

Functional and Comparative Genomic Analysis of Integrated Prophage-Like Sequences in “Candidatus Liberibacter asiaticus”

Marian Dominguez-Mirazo, Rong Jin, Joshua S. Weitz
Katherine McMahon, Editor
Marian Dominguez-Mirazo
aSchool of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
bInterdisciplinary Graduate Program in Quantitative Biosciences, Georgia Institute of Technology, Atlanta, Georgia, USA
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  • ORCID record for Marian Dominguez-Mirazo
Rong Jin
aSchool of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
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Joshua S. Weitz
aSchool of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
cSchool of Physics, Georgia Institute of Technology, Atlanta, Georgia, USA
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Katherine McMahon
University of Wisconsin—Madison
Roles: Editor
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DOI: 10.1128/mSphere.00409-19
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  • FIG 1
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    FIG 1

    Reconstruction of type 1 and 3 prophage-like sequences using AHCA1-a and FL17-a and nearby regions. (Top panel) Sequence FL17-a is formed by a type 4 sequence followed by bacterial genes and a region resembling a type 1 prophage. Joining sequences FL17-a, FL17-b, and FL17-c reconstructs a type 1 prophage sequence with the majority of its organization similar to that predicted for the integration of SC1 (7). (Bottom panel) AHCA-1 contains a type 4 sequence followed by bacterial genes and a region highly resembling a type 3 prophage. Using nearby regions in the AHCA1 genome, a type 3 prophage can be reconstructed with an organization similar to that predicted for the integration of P-JXGC-3 (13). Brown rectangles represent assembly gaps. Alignment visualizations were done using the R package genoPlotR (v0.8.9).

  • FIG 2
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    FIG 2

    Gene composition in prophage-like sequences. A presence-absence heatmap of predicted pangenome proteins for the prophage-like sequences and phage available in public databases is shown. A clustering approach was used to obtain gene content relationships between sequences. Colors denote sequence classification as follows: red, type 1; blue, type 2; green, type 3; yellow, type 4. Sequences from the same strain that were classified as the same phage type, e.g., FL17 type 1 and TX2351 type 2, were used as a single phage for gene content analysis. Unclassified sequences were excluded from the analysis.

  • FIG 3
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    FIG 3

    Annotation of representative sequence Ishi-1-a of type 4. The figure represents predicted CDS of Ishi-1-a, with ORFs color coded to predicted functions.

  • FIG 4
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    FIG 4

    Presence of prophage-like sequence type 4 in related “Candidatus Liberibacter” species. The alignment shows a comparison of type 4 prophage-like sequence Ishi-1-a to genomes of “Ca. Liberibacter africanus” ( GCA_001021085.1) and “Ca. Liberibacter americanus” ( GCA_000496595.1).

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    “Ca. Liberibacter asiaticus” genome informationa

    TABLE 1
    • ↵a Characteristics of the 15 publicly available “Ca. Liberibacter asiaticus” genomes are indicated as follows: strain, geographic origin, GenBank accession number, number of contigs, sequence length, G+C content, and associated phage types. Dashes (—) in the contig column indicate complete (circularized) genomes. Phage types with asterisks belong to phages with publicly available genomes (Table 2).

  • TABLE 2

    “Ca. Liberibacter asiaticus” phage genome informationa

    TABLE 2
    • ↵a Characteristics of the 5 publicly available genomes of “Ca. Liberibacter asiaticus” phages are indicated as follows: phage name, associated “Ca. Liberibacter asiaticus” strain, GenBank accession number, number of contigs, sequence length, G+C content, and phage type. Dashes (—) in the contig column correspond to closed genomes.

  • TABLE 3

    Putative characteristics of prophage sequencesa

    TABLE 3
    • ↵a Characteristics of the sequences predicted by Virsorter and PHASTER are indicated as follows: “Ca. Liberibacter asiaticus” strain, sequence ID, the contig in which the sequence was found, the position in contig, the sequence length, and percent G+C content. Dashes (—) in the contig column indicate that the corresponding genome is fully assembled.

  • TABLE 4

    Classification of novel prophage-like sequences into types 1, 2, and 3a

    TABLE 4
    • ↵a The novel predicted sequences were aligned against representative phages SC1, SC2, and P-JXGC-3 of types 1, 2, and 3. Coverage (C) values corresponding to two-way local alignments are presented in this table. Blue, mustard, and pink cells stand for high, intermediate, and low alignment values. Note that the threshold values used to classify coverage (C) vary according to sequence length and position in BLAST (either query or target) (see Materials and Methods). White cells with “NA” entries represent absence of significant hits. Sequences were categorized as type 1 (red), type 2 (blue), or type 3 (green) sequences; unclassified sequences with resemblance to the representative phages (black); or unclassified without resemblance (gray).

  • TABLE 5

    Resemblance between new type 4 sequencesa

    TABLE 5
    • ↵a Data represent results of comparisons of 12 predicted sequences that did not resemble any of the representative phages of types 1, 2, and 3. Coverage (C) values corresponding to two-way local alignments are presented in this table. Blue, mustard, and pink cells stand for high, intermediate, and low values, respectively (see Materials and Methods).

  • TABLE 6

    Putative characteristics and classification of prophage sequencesa

    TABLE 6
    • ↵a Characteristics of the predicted sequences are indicated as follows: sequence ID, length, G+C content, name (either previously assigned or assigned following the scheme proposed in reference 12), and prophage or prophage-like sequence type. Asterisks (*) mark sequences AHCA1-a/F1 and AHCA1-a/F2, which represent different fragments of sequence AHCA1-a, or sequences FL17-a/F1 and FL17-a/F2, which represent different fragments of sequence FL17-a.

  • TABLE 7

    “Ca. Liberibacter asiaticus” genome information adding new prophage-like sequencesa

    TABLE 7
    • ↵a Characteristics of the 15 publicly available “Ca. Liberibacter asiaticus” genomes are indicated as follows: strain, geographic origin, GenBank accession number, number of contigs, sequence length, G+C content, and associated prophage types. Prophage types identified in this study are indicated in bold and italics. Dashes (—) in the number of contigs column indicate complete (circularized) genomes.

Supplemental Material

  • Figures
  • Tables
  • TABLE S1

    Resemblance of new type 4 sequences. Results of cross-comparisons of the 12 predicted sequences that did not resemble any of the representative phages of types 1, 2, and 3 are presented. Putative prophage sequences AHCA1-a and FL17-a were cleaved, and the fragment from each resembling the other sequences was used. Identity (I) and coverage (C) values of two-way local alignments are presented on this table. Blue, mustard, and pink cells stand for high, intermediate, and low values, respectively (see Materials and Methods). All sequences were classified as new prophage-like sequence type 4. Download Table S1, DOCX file, 0.2 MB.

    Copyright © 2019 Dominguez-Mirazo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S2

    AHCA1-a gene function. ORFs predicted for AHCA1-a were annotated using BLASTp against the nonredundant database. Information includes gene start and end positions, UniRef ID, and predicted gene function. The corresponding locus_tag from the GenBank AHCA1 genome annotation is presented in the succeeding columns with the locus_tag ID, start and end positions in the bacterial genome, and annotated function. Note that some ORFs lack a corresponding locus_tag and that some locus_tags lack a corresponding ORF. Download Table S2, DOCX file, 0.2 MB.

    Copyright © 2019 Dominguez-Mirazo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

  • TABLE S3

    Ishi-1-a gene function. ORFs predicted for Ishi-1-a were annotated using BLASTp against the nonredundant database. Information includes gene start and end positions in Ishi-1-a, UniRef ID, and predicted gene function. The corresponding locus_tag from the GenBank Ishi-1-a genome annotation is presented in the succeeding columns with the locus_tag ID, start and end positions in the bacterial genome, and annotated function. Note that some ORFs lack a corresponding locus_tag and that some locus_tags lack a corresponding ORF. Download Table S3, DOCX file, 0.2 MB.

    Copyright © 2019 Dominguez-Mirazo et al.

    This content is distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Functional and Comparative Genomic Analysis of Integrated Prophage-Like Sequences in “Candidatus Liberibacter asiaticus”
Marian Dominguez-Mirazo, Rong Jin, Joshua S. Weitz
mSphere Nov 2019, 4 (6) e00409-19; DOI: 10.1128/mSphere.00409-19

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Functional and Comparative Genomic Analysis of Integrated Prophage-Like Sequences in “Candidatus Liberibacter asiaticus”
Marian Dominguez-Mirazo, Rong Jin, Joshua S. Weitz
mSphere Nov 2019, 4 (6) e00409-19; DOI: 10.1128/mSphere.00409-19
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    • ABSTRACT
    • INTRODUCTION
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KEYWORDS

One Health
bioinformatics
environmental microbiology
microbial ecology
phage ecology
phytopathology
plant pathogens

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