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Editor's Pick Research Article | Ecological and Evolutionary Science

Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen

Ferran Garcia-Pichel, Jonathan Lombard, Tanya Soule, Sean Dunaj, Steven H. Wu, Martin F. Wojciechowski
Stephen J. Giovannoni, Editor
Ferran Garcia-Pichel
aSchool of Life Sciences, Arizona State University, Tempe, Arizona, USA
bCenter for Fundamental and Applied Microbiomics, Biodesign Institute, Arizona State University, Tempe, Arizona, USA
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Jonathan Lombard
cDepartment of Cellular and Molecular Biology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden
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Tanya Soule
dDepartment of Biology, Purdue University, Fort Wayne, Indiana, USA
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Sean Dunaj
dDepartment of Biology, Purdue University, Fort Wayne, Indiana, USA
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Steven H. Wu
eCenter for Personalized Diagnostic, Biodesign Institute, Arizona State University, Tempe, Arizona, USA
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Martin F. Wojciechowski
aSchool of Life Sciences, Arizona State University, Tempe, Arizona, USA
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Stephen J. Giovannoni
Oregon State University
Roles: Editor
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DOI: 10.1128/mBio.00561-19
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  • FIG 1
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    FIG 1

    Genomic organization of the cyanobacterial scytonemin operon. Gene nomenclature is based on the annotation of Nostoc punctiforme ATCC 29133. Core biosynthetic genes are shown in yellow. Regulatory genes are shown in blue. Genes shown in black or gray involve a region dedicated to monomer export, and genes shown in various shades of purple/pink code for dedicated aromatic amino acid biosynthetic (AAAB) genes that supply biosynthetic precursors.

  • FIG 2
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    FIG 2

    Phylogeny derived from BEAST analyses of TrpD amino acid sequences supports an origin of a scytonemin-associated clade in a single internal duplication of housekeeping genes, shown as exemplary of the two phylogenies (TrpB and TrpC) supporting such an origin. The corresponding phylogeny for TrpC is in Fig. S8. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the oldest clade containing scytonemin-associated homologs.

  • FIG 3
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    FIG 3

    Phylogeny derived from BEAST analyses of TyrA amino acid sequences supports an origin by lateral transfer from bacterial phyla other than cyanobacteria of the homologs in the scytonemin operon. It is shown as exemplary of the three phylogenies (AAAB loci trpE, aroB, and tyrA) supporting such an origin. Phylogenies for the other genes are found in Fig. S5 and S9. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5.

  • FIG 4
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    FIG 4

    Phylogeny derived from BEAST analyses of TrpB amino acid sequences supports an origin of scytonemin-associated homologs by more than one internal duplication of housekeeping genes, shown as exemplary of the three phylogenies (trpB, trpA, and aroG) supporting such an origin. Phylogenies for the other genes are found in Fig. S6 and S7). Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the oldest clade containing scytonemin-associated homologs.

  • FIG 5
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    FIG 5

    Time estimates for the origin of cyanobacteria (blue-green) and scytonemin (orange) derived from relaxed molecular clock models applied to the phylogeny of gene products associated with the scytonemin operon. Each of the lower 5 boxes corresponds to a gene product as marked. In each of these boxes, the upper estimates used an age of 0.9 billion years for the common ancestor of all heterocystous cyanobacteria, whereas the lower estimates used an age of 2.1 billion years. Error bars are 95% CI for each estimate. The two uppermost boxes include averages of single-gene estimates for each of the two age scenarios (Means) or for all estimates (Grand Means).

  • FIG 6
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    FIG 6

    Phylogeny derived from BEAST analyses of full 16S rRNA sequences of cyanobacteria. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the clades encompassing scytonemin-operon containing genomes.

Tables

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  • TABLE 1

    Summary of phylogenetic results for the evolution of aromatic amino acid biosynthesis loci contained in the scytonemin operon of cyanobacteria as determined from model-based Bayesian analyses of relevant locus-specific data sets

    LocusWhether orthologs form
    monophyletic group
    Whether scytonemin clade(s)a originate(s)
    within cyanobacterial phylogeny
    Housekeeping phylogeny consistent
    with cyanobacterial phylogenyb
    trpBUnclearYesYes
    trpCYesYesYes
    trpDYesYesYes
    trpANo, two cladesYesYes
    aroGNo, multiple cladesYesYes
    trpEYesNo, lateral transferYes
    aroBYesNo, lateral transferYesc
    tyrAYesNo, lateral transferYes
    • ↵a Including a clade of supernumerary and scytonemin operon remnant copies.

    • ↵b See text for criteria.

    • ↵c However, it contains two clades of heterocystous cyanobacteria.

Supplemental Material

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  • FIG S1

    Phylogenetic relationships of cyanobacteria derived from neighbor-joining analysis of amino acid sequences of the core scytonemin genes scyABCF. Numbers next to nodes represent nonparametric bootstrap support values based on 1,000 replicates. Scytonemin-operon homolog sequences are demarcated by the orange bar, and most closely related genes are demarcated from other bacteria by the blue bar. Download FIG S1, PDF file, 0.3 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S2

    Phylogenetic relationships of cyanobacteria derived from neighbor-joining analysis of amino acid sequences of the aroB (114 taxa, 219 characters) and aroG (78 taxa, 341 characters) genes. Numbers next to selected nodes represent nonparametric bootstrap support values based on 500 replicates, but only those above 70% are marked. Scytonemin-operon gene homolog sequences are shown in blue type, and supernumerary homologs (beyond housekeeping and scytonemin associated) and those in remnant scytonemin operons are in green type. Download FIG S2, PDF file, 0.1 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S3

    Phylogenetic relationships of cyanobacteria derived from neighbor-joining analysis of amino acid sequences of the trpA (89 taxa, 235 characters), trpB (89 taxa, 395 characters), trpC (95 taxa, 233 characters), and trpD (84 taxa, 294 characters) genes. Numbers next to selected nodes represent nonparametric bootstrap support values based on 500 replicates, but only those above 70% are marked. Scytonemin-operon gene homolog sequences are shown in blue type, and supernumerary homologs (beyond housekeeping and scytonemin associated) and those in remnant scytonemin operons are in green type. Download FIG S3, PDF file, 0.2 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S4

    Phylogenetic relationships of cyanobacteria derived from neighbor-joining analysis of amino acid sequences of the trpE (94 taxa, 354 characters) and tyrA (83 taxa, 137 characters) genes. Numbers next to selected nodes represent nonparametric bootstrap support values based on 500 replicates, but only those above 70% are marked. Scytonemin-operon gene homolog sequences are shown in blue type, and supernumerary homologs (beyond housekeeping and scytonemin associated) and those in remnant scytonemin operons are in green type. Download FIG S4, PDF file, 0.1 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S5

    Phylogeny for scytonemin-dedicated AAAB genes of AroB amino acid sequences derived from BEAST analyses. Entries in blue type correspond to homologs found within full scytonemin operons. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. Download FIG S5, PDF file, 0.6 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S9

    Phylogeny derived from BEAST analyses of TrpE amino acid sequences for scytonemin-dedicated AAAB genes. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. Download FIG S9, PDF file, 0.5 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S6

    Phylogeny derived from BEAST analyses of AroG amino acid sequences for scytonemin-dedicated AAAB genes. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the oldest clade containing scytonemin-associated homologs. Download FIG S6, PDF file, 0.5 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S7

    Phylogeny derived from BEAST analyses of TrpA amino acid sequences for scytonemin-dedicated AAAB genes. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow correspond to those found in operon remnants operons or to supernumerary copies. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the oldest clade containing scytonemin-associated homologs. Download FIG S7, PDF file, 0.5 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • FIG S8

    Phylogeny derived from BEAST analyses of TrpC amino acid sequences for scytonemin-dedicated AAAB genes. Entries in blue type correspond to homologs found within full scytonemin operons. Those marked by a blue arrow were found in remnant scytonemin operons or correspond to supernumerary homologs. Bayesian posterior probabilities (BPP) at the nodes are color coded as follows: red for BPP ≥ 0.8, pink for 0.8 ≥ BPP ≥ 0.5, and white for BPP ≤ 0.5. The red arrow marks the node corresponding to the most recent common ancestor of the oldest clade containing scytonemin-associated homologs. Download FIG S8, PDF file, 0.6 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

  • TEXT S1

    (A) Genomes used in the analyses. (B) Sequences from Nostoc punctiforme PCC 73102 (ATCC 29133) used as seeds in the BLAST analyses. Download Text S1, PDF file, 0.1 MB.

    Copyright © 2019 Garcia-Pichel et al.

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

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Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
Ferran Garcia-Pichel, Jonathan Lombard, Tanya Soule, Sean Dunaj, Steven H. Wu, Martin F. Wojciechowski
mBio May 2019, 10 (3) e00561-19; DOI: 10.1128/mBio.00561-19

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Timing the Evolutionary Advent of Cyanobacteria and the Later Great Oxidation Event Using Gene Phylogenies of a Sunscreen
Ferran Garcia-Pichel, Jonathan Lombard, Tanya Soule, Sean Dunaj, Steven H. Wu, Martin F. Wojciechowski
mBio May 2019, 10 (3) e00561-19; DOI: 10.1128/mBio.00561-19
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KEYWORDS

UV photobiology
cyanobacteria
deep evolution
secondary metabolism

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