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Research Article | Applied and Environmental Science

Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments

Asier Zaragoza-Solas, Francisco Rodriguez-Valera, Mario López-Pérez
Jillian Petersen, Editor
Asier Zaragoza-Solas
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Alicante, Spain
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Francisco Rodriguez-Valera
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Alicante, Spain
bLaboratory for Theoretical and Computer Research on Biological Macromolecules and Genomes, Moscow Institute of Physics and Technology, Dolgoprudny, Russia
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Mario López-Pérez
aEvolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, Alicante, Spain
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Jillian Petersen
University of Vienna
Roles: Editor
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DOI: 10.1128/mSystems.00905-19
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  • FIG 1
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    FIG 1

    Unrooted phylogenomic tree of concatenated conserved proteins (terminase small subunit, terminase large subunit, tail tube monomer, tail tube monomer, baseplate wedge protein gp8, and VrlC protein) found in pelagimyophages (PMPs) and in the cyanomyophage outgroup. The reference cultured PMP is highlighted in red. The size (in kilobases) of each MAVG is shown in parentheses next to each branch, with complete PMP MAVGs marked with solid circles.

  • FIG 2
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    FIG 2

    Alignment of pelagimyophage genomes (tblastx, 30% identity). (A) Whole-genome alignment of two PMP-A group genomes. The different modules and hypervariable regions are labeled with black lines over the genomes, while the host recognition module (HRC) is highlighted in red. (B) Whole-genome alignment of a complete representative of each PMP group. (C) Close-up view of the HRC. Genes are colored according to their predicted function.

  • FIG 3
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    FIG 3

    Alignment of pelagimyophage and cyanomyophage (CMP) phages (tblastx, 30% identity). Gene modules are labeled with black lines over the genomes, with the host recognition cluster highlighted in red. (A) Alignment of two CMPs. (C) Alignment of three PMPs from group PMP-B with a similar HRC.

  • FIG 4
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    FIG 4

    Recruitment of pelagimyophages. (A) Relative abundance of PMPs reads in Mediterranean, Geotraces, and Tara Oceans metagenomes and viromes is shown along with the abundances of SAR11 bacteria, SAR11 podoviruses, and Cyanobacteria and their myophages. The horizontal axis shows the normalized count of reads per kilobase pair of genome and megabase pair of metagenome (RPKM), while the vertical axis shows the sampling stations (like in reference 33). (B) Heatmap of abundance of PMPs in freshwater and Mediterranean cellular metagenomes and viromes. Normalization of the abundance was performed by calculating RPKG (reads recruited per kilobase of the genome per gigabase of the metagenome).

Tables

  • Figures
  • Supplemental Material
  • TABLE 1

    Genomic features for the pelagimyophages analyzed in this study

    TABLE 1
    • ↵a Igs, intergenic spacer.

    • ↵b How completeness was found is shown is parentheses: Cu, cultivated; Al, alignment; TR, terminal repeats.

    • ↵c Protein matches, based on BLASTN hits with at least 70% similarity and an alignment length between 70% and 130% of the length of the smaller protein.

    • ↵d M, marine; F, freshwater.

    • ↵e C, culture; MG, metagenome; V, virome.

Supplemental Material

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  • Tables
  • FIG S1

    Genome mining pipeline. (A) Workflow describing the steps used in the genome mining process, shown colored based on the step. (B) Contigs remaining in the analysis after each step, long with the average contig size. Each step includes a key to the workflow in panel A. Download FIG S1, PDF file, 0.2 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • TABLE S1

    Metagenomic database samples utilized in this study. Download Table S1, PDF file, 0.4 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • TABLE S2

    Pelagimyophage recruitment values for Tara Oceans metagenomes and viromes. Normalization of the abundance was performed by calculating RPKG (reads recruited per kilobase of the genome per gigabase of the metagenome). Download Table S2, XLSX file, 0.04 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • TABLE S3

    Pelagimyophage recruitment values for Geotraces metagenomes. Normalization of the abundance was performed by calculating RPKG (reads recruited per kilobase of the genome per gigabase of the metagenome). Download Table S3, XLSX file, 0.1 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • FIG S2

    Heatmap of abundance of pelagimyophages in GEOTRACES Cruise GA3 samples. Download FIG S2, PDF file, 0.2 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • FIG S3

    (A) Linear recruitments of various pelagimyophages against various metagenomes and viromes. The host recognition cluster (HRC) is indicated by a red rectangle. (B) Isoelectric point versus density plot of marine (HTVC008M) and freshwater (PMP-MAVG-15) pelagimyophages. (C) Genome alignment of HTVC008M and PMP-MAVG-15. Genomic modules are indicated by black bars over the genomes, with the HRC highlighted in red. Download FIG S3, PDF file, 2.5 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • FIG S4

    (A) Cooccurrence networks of cyanomyophage and pelagimyophage genomes. Each node represents a protein cluster (PC), while each edge indicates that the two nodes it connects are present in the same operon in at least a pair of genomes. Edge thickness indicates the number of genomes the two PCs are present in the same operon. Each node is colored according to its predicted function. (B) Phylogenetic trees of two curli operon proteins (CsgF and CsgG) from pelagimyophages, Alphaproteobacteria, and Gammaproteobacteria. Pelagimyophage genes are highlighted in red. Download FIG S4, PDF file, 0.2 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • FIG S5

    Phylogenetic terminase tree. The branch with the reference terminase genes is shown in red. Download FIG S5, PDF file, 0.1 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • TABLE S4

    Protein clusters (PCs) with size of >10 genes and a log fold difference of at least 1. Normalized gene counts were calculated as follows: (total number of genes in all genomes of the group/total genomes in the group). Download Table S4, PDF file, 0.2 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

  • TABLE S5

    AMGs detected in the analyzed genomes. Download Table S5, PDF file, 0.2 MB.

    Copyright © 2020 Zaragoza-Solas et al.

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

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Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments
Asier Zaragoza-Solas, Francisco Rodriguez-Valera, Mario López-Pérez
mSystems Feb 2020, 5 (1) e00905-19; DOI: 10.1128/mSystems.00905-19

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Metagenome Mining Reveals Hidden Genomic Diversity of Pelagimyophages in Aquatic Environments
Asier Zaragoza-Solas, Francisco Rodriguez-Valera, Mario López-Pérez
mSystems Feb 2020, 5 (1) e00905-19; DOI: 10.1128/mSystems.00905-19
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    • ABSTRACT
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KEYWORDS

Fonsibacter
pelagiphages
SAR11
genome-resolved metagenomics
myophages

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