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Sawyeria marylandensis (Heterolobosea) Has a Hydrogenosome with Novel Metabolic Properties

Maria José Barberà, Iñaki Ruiz-Trillo, Julia Y. A. Tufts, Amandine Bery, Jeffrey D. Silberman, Andrew J. Roger
Maria José Barberà
1Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada
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Iñaki Ruiz-Trillo
1Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada
2Departament de Genètica & Institut de Recerca en Biodiversitat (Irbio), Universitat de Barcelona, Barcelona, Spain
3Institució Catalana per la Recerca i Estudis Avançats (ICREA), Parc Científic de Barcelona, Barcelona, Spain
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Julia Y. A. Tufts
1Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada
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Amandine Bery
2Departament de Genètica & Institut de Recerca en Biodiversitat (Irbio), Universitat de Barcelona, Barcelona, Spain
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Jeffrey D. Silberman
1Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada
4Department of Biological Sciences, University of Arkansas, Fayetteville, Arkansas
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Andrew J. Roger
1Centre for Comparative Genomics and Evolutionary Bioinformatics, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, NS, Canada
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  • For correspondence: Andrew.Roger@dal.ca
DOI: 10.1128/EC.00122-10
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  • Fig. 1.
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    Fig. 1.

    Maximum-likelihood (ML) phylogenetic trees of mitochondrial Hsp70 (A), cysteine desulfurase (IscS) (B), [FeFe]-hydrogenase (C), and pyruvate:ferredoxin oxidoreductase (D). Trees were constructed using RAxML with a WAG+Γ model of evolution. Bootstrap support values above 50 are shown over branches.

  • Fig. 2.
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    Fig. 2.

    Comparison of the N termini of several different protein homologues from Sawyeria and several representative eukaryote sequences, showing the putative targeting peptides. Aligned bacterial homologues, which do not contain targeting peptides, are also shown. Most of the putative targeting peptides of Sawyeria were not predicted by automated software (see Materials and Methods and the main text).

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    Fig. 3.

    Transmission electron micrographs of Sawyeria marylandensis. (A) Full view of a Sawyeria marylandensis cell. (B) Partial view of an S. marylandensis cell showing the three different shapes of the mitochondrion-related organelle. (C) S. marylandensis cell with several hydrogenosomes. (D) An inset view of picture C. (E) View of a hydrogenosome of S. marylandensis. (F) Close view showing double-membrane structure of the organelle.

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    Fig. 4.

    3D reconstruction of shape of Sawyeria hydrogenosomes derived from serial sectioning transmission electron microscopy. The bean-shaped MRO is about 1.8 μm tall, 1.5 μm long, and 0.840 μm wide. The cup-shaped MRO is 1.5 μm tall and 1.65 μm wide. See the main text for more details.

Tables

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  • Table 1.

    Mitocondrial/hydrogenosomal proteins in Sawyeria marylandensis and comparison with N. gruberi, T. vaginalis, and G. intestinalisa

    Category or S. marylandensis mitochondrial/hydrogenosomal proteinAccession no.dN-terminal extensioneAnnotationf
    TBestDBNCBINgTvGi
    Energy metabolism
        [FeFe]-hydrogenaseb EF612752 (SmHydA)Yes+++
    EF612753 (SmHydB)
        Pyruvate:ferredoxin oxidoreductase (PFO)b EF612751 Yes−++
        Alpha-succinyl-CoA synthetasebSML00000322 EF612760 Yes++−
        Beta-succinyl-CoA synthetasebSML00000048 EF612761 Yes++−
        2Fe-2S FerredoxincSML00003510EC818301?+++
        Putative glycerol kinasecSML00001707EC823814?+−+
    Fe-hydrogenase assembly
        HydGbSML00000047 EF612762 Yes++−
        HydFcSML00000703EC826105?++−
    Mitochondrial carrier family
        Putative ATP/ADP Carrier (AAC)bSML00000111EC824912No++−
    SML00000209EC825377
    Mitochondrial import pathway
        Cpn60b EU233795 Yes+++
        Hsp70b EF612755 Yes+++
        Cpn10b EF612758 No++−
        TOM34cSML00000787EC825338?−/+−−
        TIM 23cSML00000812EC826107?+−−
        TIM 44cSML00000628EC825535?+−−
    Mitochondrial respiratory complex I
        51 kDa (NuoF)b EF612754 Yes++−
        24 kDa (NuoE)cSML00003413EC824286?++−
    ISC pathway
        IscSb EF612756 Yes+++
        IscUb EF612757 ?+++
        FrataxincSML00000479EC823663?+++
    Fatty acid metabolism
        Propionyl-CoA carboxylase alpha chaincSML00000070EC826322?+−−
        Propionyl-CoA carboxylase beta chaincSML00000244EC825818?+−−
        3-Ketoacyl-CoA thiolasecSML00000148EC826272+−−
    Amino acid metabolism
        Dihydrolipoamide dehydrogenase (L protein)bSML00002324 EF612759 Yes+−−
        Glycine cleavage system HcSML00003411EC819138?++−
        Glycine cleavage system PcSML00003181EC821614?++−
        4-Aminobutyrate transaminasecSML00000492EC825405?+−−
        Methylmalonyl-CoA mutasecSML00000635EC825225?+−−
        Serine hydroxymethyltransferasecSML00001624EC824484?++−
        Branched chain ketoacid dehydrogenase E1, alpha polypeptidecSML00000388EC826530?+−−
    SML00002275EC817751
        Branched-chain alpha-keto acid dehydrogenase E1-beta subunitcSML00001068EC825728?+−−
        Lipoamide acyltransferase (branched-chain alpha-keto acid dehydrogenase complex) E2cSML00000474EC826090?+−−
        Glutamate dehydrogenasecSML00000006EC826618?+++
        Alanine aminotransferasecSML00000316EC825413?+−−
        Aspartate aminotransferasecSML00001965EC817939?+++
        Ornithine carbamoyltransferasecSML00001073EC825834?−/+++
        Putative delta-1-pyrroline-5-carboxylate dehydrogenasecSML00000009EC826523?+−−
        Putative glutaryl-CoA dehydrogenasecSML00001691EC823693?+−−
        2-Amino-3-ketobutyrate coenzyme A ligasecSML00000023EC826214?+−−
    Other functions
        Thioredoxin reductase 2cSML00002472EC820868?+++
        NADH-cytochrome b5 reductasecSML00002452EC819124?+−−
        Succinate semialdehyde dehydrogenasecSML00000871EC822494?−/+−−
        Dynamin like proteincSML00000756EC822881?+++
    • ↵a Hits confirmed by BLAST (E < 10−5) to NCBI and PFAM.

    • ↵b Phylogeny shown in Fig. 1 or the supplemental material.

    • ↵c Automatic annotation as obtained by the AnaBench pipeline (http://anabench.bcm.umontreal.ca/anabench/ ).

    • ↵d For those genes fully sequenced, NCBI accession numbers are provided in bold. For the rest, TBestDB accession numbers are provided for the contigs plus an additional NCBI accession number for a representative EST of the contig.

    • ↵e ? indicates an incomplete sequence at the N terminus.

    • ↵f Ng, Naegleria gruberi; Tv, Trichomonas vaginalis; Gi, Giardia intestinalis. “−/+” indicates that a potential distant homolog of the protein was found but its assignment to the specific protein family named could not be confirmed by reciprocal BLAST.

Additional Files

  • Figures
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  • Supplemental material

    Files in this Data Supplement:

    • Supplemental file 3 - Nine supplemental figures depicting maximum likelihood phylogenetic trees of proteins mentioned in the manuscript.
      PDF file, 576K.
    • Supplemental file 1 - Supplemental video 1 depicting 3D reconstruction of Sawyeria marylandensis hydrogenosomes from serial sectioning in transmission electron microscopy.
      Zipped GIF file, 2.7MB.
    • Supplemental file 2 - Supplemental video 2 depicting Sawyeria marylandensis under fluorescence microscopy.
      Zipped GIF file, 3.5MB.
    • Supplemental file 4 - Legends to supplemental figures and videos.
      MS Word document, 29K.
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Sawyeria marylandensis (Heterolobosea) Has a Hydrogenosome with Novel Metabolic Properties
Maria José Barberà, Iñaki Ruiz-Trillo, Julia Y. A. Tufts, Amandine Bery, Jeffrey D. Silberman, Andrew J. Roger
Eukaryotic Cell Dec 2010, 9 (12) 1913-1924; DOI: 10.1128/EC.00122-10

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Sawyeria marylandensis (Heterolobosea) Has a Hydrogenosome with Novel Metabolic Properties
Maria José Barberà, Iñaki Ruiz-Trillo, Julia Y. A. Tufts, Amandine Bery, Jeffrey D. Silberman, Andrew J. Roger
Eukaryotic Cell Dec 2010, 9 (12) 1913-1924; DOI: 10.1128/EC.00122-10
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KEYWORDS

Eukaryota
Hydrogenase
Mitochondria
Pyruvate Synthase

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