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Research Article

Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “Candidatus Synechococcus spongiarum”

Zhao-Ming Gao, Yong Wang, Ren-Mao Tian, Yue Him Wong, Zenon B. Batang, Abdulaz M. Al-Suwailem, Vladimir B. Bajic, Pei-Yuan Qian
Maria Gloria Dominguez Bello, Editor
Zhao-Ming Gao
aKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of China
bKey Laboratory of Marine Biogenetic Resources, Third Institute of Oceanography, State Oceanic Administration (SOA), Xiamen, People’s Republic of China
cSanya Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Hainan, People’s Republic of China
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Yong Wang
aKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of China
cSanya Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Hainan, People’s Republic of China
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Ren-Mao Tian
aKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of China
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Yue Him Wong
aKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of China
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Zenon B. Batang
dCoastal and Marine Resources Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
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Abdulaz M. Al-Suwailem
dCoastal and Marine Resources Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
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Vladimir B. Bajic
eComputational Bioscience Research Center (CBRC) and Computer, Electrical and Mathematical Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia
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Pei-Yuan Qian
aKAUST Global Collaborative Research Program, Division of Life Science, The Hong Kong University of Science and Technology, Kowloon, Hong Kong, People’s Republic of China
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Maria Gloria Dominguez Bello
New York University School of Medicine
Roles: Editor
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DOI: 10.1128/mBio.00079-14
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  • FIG 1 
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    FIG 1 

    Neighbor-joining phylogenetic tree of strain SH4 and closely related cyanobacterial strains based on partial 16S rRNA genes (1,100 bp). CSS, cluster of “Ca. Synechococcus spongiarum.” Bootstrap values based on 1,000 replications are shown as percentages at branch angles. Scale bar indicates 1% estimated sequence divergence.

  • FIG 2 
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    FIG 2 

    Phylogenomic inference of “Ca. Synechococcus spongiarum” SH4. (a) Maximum-likelihood phylogenomic tree using 31 concatenated conserved proteins of SH4 and cyanobacterial strains. The branches were colored according to the bootstrap values, ranging from purple (80%) to red (100%). Scale bar indicates 10% estimated sequence divergence. (b) ANI values plus correlation indexes of tetranucleotide frequency between SH4 and closely related Synechococcus, Prochlorococcus, Cyanobium cluster Synechococcus, and other cyanobacterial strains revealed differences in their genome composition. (c) GC content and genome size of SH4 and other cyanobacterial strains.

  • FIG 3 
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    FIG 3 

    Schematic overview of the methionine metabolism pathway in “Ca. Synechococcus spongiarum” SH4. Red and green labels indicate the absence and presence, respectively, of that enzyme in SH4.

  • FIG 4 
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    FIG 4 

    Abundance of photosynthetic genes in “Ca. Synechococcus spongiarum” SH4 and related cyanobacteria strains based on KEGG orthology annotation. The identities of the cyanobacterial strains are described in Table 1.

  • FIG 5 
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    FIG 5 

    Genes of “Ca. Synechococcus spongiarum” SH4 and related cyanobacterial strains important for resistance to oxidative stress, antibiotics, and environmental toxins based on SEED/Subsystems annotation. See details in Tables S1 and S2. The identities of the cyanobacterial strains are described in Table 1.

  • FIG 6 
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    FIG 6 

    Schematic of mode of life of the sponge symbiont “Ca. Synechococcus spongiarum.” The schematic figure was deduced from the genomic analysis of the draft genome of strain SH4.

Tables

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  • TABLE 1 

    General features and functional comparison of “Candidatus Synechococcus spongiarum” SH4 and related picocyanobacterial strains

    Genome feature or gene functionValue for indicated taxona
    12345678
    Genome recovery~90%FDDFFDF
    Genome size (Mbp)1.662.222.583.042.611.752.833.34
    No. of essential genes96106104106105106105106
    % GC content63.460.864.565.452.536.468.768.7
    % Coding density87.594.292.788.487.289.387.689.5
    No. of genes in KEGG pathways
        Photosynthesis4760646164535759
        Antenna proteins242818232882117
        TCA cycles1098118111111
        DNA replication1313131413131514
        DNA repair3138414738364041
        Cysteine/methionine metabolism1021222419172124
    No. of genes in SEED/subsystems
        Response to oxidative stress1228263226212931
        Resistance to antibiotics and toxins82222282393036
        CPS and EPS biosynthesis31313161081917
        Gram-negative cell wall71412149102017
        Peptidoglycan biosynthesis1615151715151716
    Eukaryotic-like domain
        Fibronectin type III domain20010000
        AR170000000
        TPR39717161214
        LRR90000200
    • ↵a Taxa: 1, “Ca. Synechococcus spongiarum” SH4; 2, Synechococcus sp. strain RCC307; 3, Synechococcus sp. strain RS9917; 4, Synechococcus sp. strain WH 5701; 5, Synechococcus sp. strain CC9311; 6, P. marinus CCMP137; 7, Cyanobium sp. strain PCC 7001; 8, Cyanobium gracile PCC 6307. Genome recovery: F, finished genome; D, draft genome.

Supplemental Material

  • Figures
  • Tables
  • Additional Files
  • Figure S1

    High abundance of “Ca. Synechococcus spongiarum” (represented by OTU1691) in the sponge C. foliascens according to the percentage of 16S rRNA gene amplicons analyzed by tag pyrosequencing. Download Figure S1, TIF file, 2.7 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S2

    Microbial community compositions in the sponge C. foliascens revealed by 16S rRNA genes predicted from the metagenome in this study and (a) and tag pyrosequencing of 16S rRNA gene amplicons (b). Download Figure S2, TIF file, 2.1 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S3

    Genome binning of “Ca. Synechococcus spongiarum” SH4. Each circle represents a metagenomic contig with size proportional to length and colored by GC content (a) or taxonomic affiliation (b). Only contigs greater than 2 kbp in length are shown. (c) Sequence composition-independent binning of metagenomic contigs based on the coverage. (d) Principal component analysis clustering on tetranucleotide frequencies for further genome binning. Download Figure S3, TIF file, 2.8 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Figure S4

    Abundance of genes involved in amino acid metabolism pathways in “Ca. Synechococcus spongiarum” SH4 and closely related free-living cyanobacterial strains. Functional pathways are referred to the KEGG database. Download Figure S4, TIF file, 2.3 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S1

    Number of genes important for resistance to oxidative stress in SH4 and related cyanobacterial strains. Taxa: 1, “Ca. Synechococcus spongiarum” SH4; 2, Synechococcus sp. RCC307; 3, Synechococcus sp. RS9917; 4, Synechococcus sp. WH 5701; 5, Synechococcus sp. CC9311; 6, P. marinus CCMP137; 7, Cyanobium sp. PCC 7001; 8, Cyanobium gracile PCC 6307. Table S1, PDF file, 0.1 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S2

    Number of genes important for resistance to antibiotics and environmental toxins in SH4 and related cyanobacterial strains. Taxa: 1, “Ca. Synechococcus spongiarum” SH4; 2, Synechococcus sp. RCC307; 3, Synechococcus sp. RS9917; 4, Synechococcus sp. WH 5701; 5, Synechococcus sp. CC9311; 6, P. marinus CCMP137; 7, Cyanobium sp. PCC 7001; 8, C. gracile PCC 6307. Table S2, PDF file, 0.1 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

  • Table S3

    Number of genes important for DNA replication and repair in SH4 and related cyanobacterial strains. Taxa: 1, “Ca. Synechococcus spongiarum” SH4; 2, Synechococcus sp. RCC307; 3, Synechococcus sp. RS9917; 4, Synechococcus sp. WH 5701; 5, Synechococcus sp. CC9311; 6, P. marinus CCMP137; 7, Cyanobium sp. PCC 7001; 8, C. gracile PCC 6307. Table S3, PDF file, 0.2 MB.

    Copyright © 2014 Gao et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

Additional Files

  • Figures
  • Tables
  • Supplemental Material
  • Supplementary Data

    Supplementary Data

    Files in this Data Supplement:

    • Table st1, PDF - Table st1, PDF
    • Table st2, PDF - Table st2, PDF
    • Table st3, PDF - Table st3, PDF
    • Figure sf01, TIF - Figure sf01, TIF
    • Figure sf02, TIF - Figure sf02, TIF
    • Figure sf03, TIF - Figure sf03, TIF
    • Figure sf04, TIF - Figure sf04, TIF
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Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “Candidatus Synechococcus spongiarum”
Zhao-Ming Gao, Yong Wang, Ren-Mao Tian, Yue Him Wong, Zenon B. Batang, Abdulaz M. Al-Suwailem, Vladimir B. Bajic, Pei-Yuan Qian
mBio Apr 2014, 5 (2) e00079-14; DOI: 10.1128/mBio.00079-14

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Symbiotic Adaptation Drives Genome Streamlining of the Cyanobacterial Sponge Symbiont “Candidatus Synechococcus spongiarum”
Zhao-Ming Gao, Yong Wang, Ren-Mao Tian, Yue Him Wong, Zenon B. Batang, Abdulaz M. Al-Suwailem, Vladimir B. Bajic, Pei-Yuan Qian
mBio Apr 2014, 5 (2) e00079-14; DOI: 10.1128/mBio.00079-14
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