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Genomics and Proteomics

The Genome of Heliobacterium modesticaldum, a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus

W. Matthew Sattley, Michael T. Madigan, Wesley D. Swingley, Patricia C. Cheung, Kate M. Clocksin, Amber L. Conrad, Liza C. Dejesa, Barbara M. Honchak, Deborah O. Jung, Lauren E. Karbach, Ahmet Kurdoglu, Surobhi Lahiri, Stephen D. Mastrian, Lawrence E. Page, Heather L. Taylor, Zi T. Wang, Jason Raymond, Min Chen, Robert E. Blankenship, Jeffrey W. Touchman
W. Matthew Sattley
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Michael T. Madigan
2Department of Microbiology, Southern Illinois University, Carbondale, Illinois 62901
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Wesley D. Swingley
3Institute of Low Temperature Science, Hokkaido University, N19W8, Sapporo 060-0819, Japan
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Patricia C. Cheung
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Kate M. Clocksin
2Department of Microbiology, Southern Illinois University, Carbondale, Illinois 62901
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Amber L. Conrad
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
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Liza C. Dejesa
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
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Barbara M. Honchak
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Deborah O. Jung
2Department of Microbiology, Southern Illinois University, Carbondale, Illinois 62901
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Lauren E. Karbach
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Ahmet Kurdoglu
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
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Surobhi Lahiri
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Stephen D. Mastrian
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
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Lawrence E. Page
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Heather L. Taylor
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
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Zi T. Wang
1Department of Biology, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Jason Raymond
5School of Natural Sciences, University of California, Merced, California 95344
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Min Chen
6School of Biological Sciences (A08), The University of Sydney, NSW 2006 Sydney, Australia
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Robert E. Blankenship
7Departments of Biology and Chemistry, Washington University, Campus Box 1137, St. Louis, Missouri 63130
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Jeffrey W. Touchman
4Translational Genomics Research Institute, Scottsdale, Arizona 85259
8School of Life Sciences, Arizona State University,Tempe, Arizona 85287
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  • For correspondence: j.touchman@asu.edu
DOI: 10.1128/JB.00299-08
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  • FIG. 1.
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    FIG. 1.

    Circular genome map of the 3.1-Mb H. modesticaldum chromosome. The rings indicate (from outside to inside) all the genes and insertion elements, color coded by functional category (rings 1 and 2), the deviation from the average G+C content (ring 3), and the GC skew (ring 4). The approximate location of the origin of replication is at the beginning of the dnaA gene. The colors indicate the following: turquoise, small-molecule biosynthesis; yellow, central or intermediary metabolism; orange, energy metabolism; red, signal transduction; light blue, DNA metabolism; blue, transcription; purple, protein synthesis/fate; dark green, surface-associated features; gray, miscellaneous features; pink, phage and insertion elements; light green, unknown function; dark gray, conserved hypothetical proteins; black, hypothetical proteins; brown, pseudogenes.

  • FIG. 2.
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    FIG. 2.

    Putative pathway of carbon metabolism in H. modesticaldum (adapted from reference 44). A partial reverse citric acid cycle with CO2 incorporation via PEP carboxykinase is shown. The enzymes involved in the reduction of acetate to pyruvate putatively function in an oxidative direction during chemotrophic (dark) growth on pyruvate. The oxidation of pyruvate to acetyl-CoA is likely accompanied by hydrogen evolution via an [FeFe] hydrogenase. The numbers indicate the following enzymes: 1, pyruvate:ferredoxin oxidoreductase; 2, pyruvate-phosphate dikinase; 3, PEP carboxykinase; 4, oxaloacetate decarboxylase; 5, malate dehydrogenase; 6, fumarase; 7, fumarate reductase; 8, succinyl-CoA synthetase; 9, 2-oxoglutarate:ferredoxin oxidoreductase; 10, NADP-dependent isocitrate dehydrogenase; 11, aconitate hydratase; 12, AMP-forming acetyl-CoA synthetase; 13, lactate dehydrogenase.

  • FIG. 3.
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    FIG. 3.

    Schematic representation of hydrogenase and photosynthesis gene clusters in H. modesticaldum. Arrows represent individual genes and indicate the direction of transcription. (A) Putative [FeFe] hydrogenase genes in H. modesticaldum and the close phylogenetic relative P. thermopropionicum SI. As in Heliobacillus mobilis, nuoE and nuoF are fused in H. modesticaldum, suggesting that this feature may be universal in heliobacteria. Colors indicate the following: gold, NADH dehydrogenase subunits; orange, [FeFe] hydrogenase structural genes. (B) Uptake [NiFe] hydrogenase genes in related Firmicutes. The genes are located in a single operon in H. modesticaldum, whereas they are dispersed in different regions of the D. hafniense Y51 chromosome. Colors indicate the following: blue, [NiFe] hydrogenase structural genes; purple, hydrogenase expression/formation; red, hydrogenase assembly/maturation. (C) Photosynthesis gene clusters from H. modesticaldum and the purple bacterium R. capsulatus. Shared genes are outlined with bold lines. Lines indicate gene synteny, as follows: black lines, single gene rearrangements; red lines, inverted genes; blue lines, inverted genes with a gene insertion. Dashed boxes indicate R. capsulatus photosynthesis genes absent from H. modesticaldum. The colors of the arrows indicate the following: green, Bchl biosynthesis (bch); orange, carotenoid biosynthesis (crt); pink, proteobacterial reaction centers (puf) and light harvesting complexes (puh); olive, heliobacterial reaction center (psh); teal, regulatory proteins; light green, electron transport (pet); red, cofactor biosynthesis; purple, cell division and sporulation; light blue, nitrogen fixation; gray, transcription; light gray, other nonphotosynthetic genes; white, uncharacterized genes.

  • FIG. 4.
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    FIG. 4.

    Phylogenetic tree showing the relationship of concatenated bchXYZ, bchLNB, and nifHDK genes from H. modesticaldum to those of other organisms containing these genes. Although not present in H. modesticaldum, alternative nitrogenase genes, anfHDK and vnfHDK, are also included to balance the tree. Organisms containing more than one set of genes used in the comparison appear multiple times in the tree. The following organisms were included in the analysis: Anabaena siamensis strain TISTR8012, Azospirillum brasilense, Azotobacter vinelandii, Bradyrhizobium sp. strain BTAi1, Bradyrhizobium sp. strain ORS278, Chlorobaculum tepidum, Chloroflexus aurantiacus, Clostridium acetobutylicum, Clostridium pasteurianum, Clostridium kluyveri, Desulfitobacterium hafniense strain Y51, Geobacter sulfurreducens, Heliobacterium modesticaldum, Jannaschia sp. strain CCS1, Klebsiella pneumoniae, Methanothermobacter thermoautotrophicus, Methanococcus maripaludis, Methanosarcina acetivorans strain C2A, Nostoc sp. strain PCC7120, Prosthecochloris aestuarii, Rhodobacter capsulatus, Rhodopseudomonas palustris, Roseiflexus castenholzii, Roseobacter denitrificans, Synechococcus elongatus strain PCC6301, and Synechocystis sp. strain PCC6803.

  • FIG. 5.
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    FIG. 5.

    Proposed pathway of later steps in Bchl g biosynthesis in H. modesticaldum. Divinyl protochlorophyllide a is reduced to 8-vinyl chlorophyllide a by the activity of the bchLNB gene products. This is followed by the reduction of the C-7—C-8 double bond via the bchXYZ gene products, which yields C-8 vinyl bacteriochlorophyllide a. Bacteriochlorophyllide g is produced by the isomerization of the 81-vinyl group to an ethylidene group. Bchl synthetase (BchG) then catalyzes the addition of a farnesyl group, which yields the completed Bchl g.

  • FIG. 6.
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    FIG. 6.

    Diagram showing a putative pathway of electron transfer based on genetic components present in H. modesticaldum. Cyclic electron transfer has not been confirmed in heliobacteria. In addition, the reduction of NAD+ by cytoplasmic ferredoxin has not been confirmed, as a gene encoding FNR was not identified in the genome. Despite this, genes encoding all 14 subunits of NADH:quinone oxidoreductase (nuoA to nuoN) were putatively identified.

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  • TABLE 1.

    Features of the H. modesticaldum strain Ice1T (= ATCC 51547T) genome

    CharacteristicValue
    Chromosome size (bp)3,075,407
    G+C content (%)56.0
    % Genome coding87
    Total no. of ORFs3,138
    Avg ORF length (bp)882
    % ATG initiation codons62.1
    % GTG initiation codons19.1
    % TTG initiation codons18.8
    No. of rRNAs (no. of genes/no. of operons)24/8
    No. of tRNAs104
    No. of structural RNAs1
    No. of tmRNA1
    % Conserved hypothetical proteins11.1
    % Hypothetical proteins23.8
    No. of transposases70
    No. of pseudogenes8
  • TABLE 2.

    Characterization of selected gene categories of the H. modesticaldum strain Ice1T (=ATCC 51547T) genome

    CategoryNo. of genes% of genome content
    Energy and central intermediary metabolism38913.0
    Amino acid biosynthesis1133.8
    Transport1575.2
    Cofactor and prosthetic group biosynthesis1525.1
    DNA metabolism1354.5
    Transcription441.5
    Protein synthesis, modification, and degradation2478.2
    Regulatory functions and signal transduction1775.9
    Cellular processes (cell division, motility, sporulation, etc.)2739.1
    Fatty acid and phospholipid metabolism451.5
    Phage/insertion elements1234.1
    Surface features1454.8

Additional Files

  • Figures
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  • Supplemental material

    Fig. S1, BchG phylogeny of Heliobacterium modesticaldum.
    Zipped TIF file, 1.8MB.

    Files in this Data Supplement:

    • Supplemental file 1 - Fig. S1, BchG phylogeny of Heliobacterium modesticaldum.
      Zipped TIF file, 1.8MB.
    • Supplemental file 2 - Fig. S2, type I reaction center core protein phylogeny of H. modesticaldum and other phototrophs.
      Zipped TIF file, 1.3MB.
    • Supplemental file 3 - Legends to Fig. S1 and S2.
      MS Word document, 23K.
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The Genome of Heliobacterium modesticaldum, a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus
W. Matthew Sattley, Michael T. Madigan, Wesley D. Swingley, Patricia C. Cheung, Kate M. Clocksin, Amber L. Conrad, Liza C. Dejesa, Barbara M. Honchak, Deborah O. Jung, Lauren E. Karbach, Ahmet Kurdoglu, Surobhi Lahiri, Stephen D. Mastrian, Lawrence E. Page, Heather L. Taylor, Zi T. Wang, Jason Raymond, Min Chen, Robert E. Blankenship, Jeffrey W. Touchman
Journal of Bacteriology Jun 2008, 190 (13) 4687-4696; DOI: 10.1128/JB.00299-08

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The Genome of Heliobacterium modesticaldum, a Phototrophic Representative of the Firmicutes Containing the Simplest Photosynthetic Apparatus
W. Matthew Sattley, Michael T. Madigan, Wesley D. Swingley, Patricia C. Cheung, Kate M. Clocksin, Amber L. Conrad, Liza C. Dejesa, Barbara M. Honchak, Deborah O. Jung, Lauren E. Karbach, Ahmet Kurdoglu, Surobhi Lahiri, Stephen D. Mastrian, Lawrence E. Page, Heather L. Taylor, Zi T. Wang, Jason Raymond, Min Chen, Robert E. Blankenship, Jeffrey W. Touchman
Journal of Bacteriology Jun 2008, 190 (13) 4687-4696; DOI: 10.1128/JB.00299-08
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KEYWORDS

Genome, Bacterial
Gram-positive bacteria

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