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Microbial Ecology

Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea

Steven J. Hallam, Peter R. Girguis, Christina M. Preston, Paul M. Richardson, Edward F. DeLong
Steven J. Hallam
1Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-9644
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Peter R. Girguis
1Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-9644
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Christina M. Preston
1Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-9644
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Paul M. Richardson
2The Joint Genome Institute, Walnut Creek, California 94598
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Edward F. DeLong
1Monterey Bay Aquarium Research Institute, Moss Landing, California 95039-9644
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  • For correspondence: delong@mbari.org
DOI: 10.1128/AEM.69.9.5483-5491.2003
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  • FIG. 1.
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    FIG. 1.

    Distance comparison of SSU rRNA and mcrA-based phylogenetic trees of environmental clones and primary methanogenic lineages. Bootstrap values are based on 1,000 replicates each (neighbor joining on top and parsimony on bottom) and are shown for branches with greater than 50% support. Methanocaldococcus spp. were used as the out group reference. ER, Eel River; MC, Monterey Canyon; AMIS, microcosm; BR, Blake Ridge. Boldface identifies clones identified and sequenced in this study. Red highlights ANME-2 group members, and blue highlights ANME-1 group members. Scale bars represent 0.05 nucleotide or amino acid substitution per site.

  • FIG.2.
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    FIG.2.

    (A) Schematic depiction of mcrA and mrt operon structure for MOA-associated fosmids and major methanogenic lineages. The mcrA operon typically consists of mcrBDCGA. The mrt operon structure varies between lineages. Scale bar, 500 bp. (B) Gene trees for mcrA and mrt subunits depicted in A. Abbreviations for methanogenic species harboring these genes are Mj, Methanocaldococcus jannaschii; Mv, Methanococcus vannielii; Mt, Methanothermobacter thermautotrophicus; and Mm, Methanosarcina mazei. Accession numbers for sequences used in the analyses are shown in parentheses for mcrB-Mj (NP_247836.1 ), mcrB-Mv (P07956), mcrB-Mt (NP_276296.1 ), mcrB-Mm (NP_633268.1 ), mcrC-Mj (NP_247838.1 ), mcrC-Mv (P07960), mcrC-Mt (NP_276294.1 ), mcrC-Mm (NP_633266.1 ), mcrD-Mj (NP_247837.1 ), mcrD-Mv (P07957), mcrD-Mt (NP_276295.1 ), mcrD-Mm (NP_633267.1 ), mcrG-Mj (NP_247839.1 ), mcrG-Mv (P07963), mcrG-Mt (NP_276293.1 ), mcrG-Mm (NP_633265.1 ), mcrA-Mj (NP_247840.1 ), mcrA-Mv (E27793), mcrA-Mt (NP_276292.1 ), mcrA-Mm (NP_633264.1 ), mrtB-Mj (NP_247045.1 ), mrtB-Mt (NP_276260.1 ), mrtC-Mj (NP_247058.1 ), mrtD-Mj (NP_247083.1 ), mrtD-Mt (NP_276259.1 ), mrtG-Mj (NP_247046.1 ), mrtG-Mt (NP_276258.1 ), mrtA-Mj (NP_247047.1 ), and mrtA-Mt (NP_276257.1 ). Bootstrap values are based on 1,000 replicates each (neighbor joining on top and parsimony on bottom) and are shown for branches with greater than 50% support. Trees are unrooted. Scale bars represent 50 amino acid substitutions.

  • FIG. 3.
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    FIG. 3.

    Amino acid alignment of representative environmental mcrA types and primary methanogenic lineages. Methanothermobacter thermoautotrophicus was used as the reference sequence (GenBank U10036 ). Position numbers correspond to the reference sequence. Amino acid identity at a given position is denoted by dots, and gaps are marked by dashes. Conserved amino acids are coded by color according to predicted CH3 modification (green), F430 binding (red), or coenzyme B interaction (blue).

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  • TABLE 1.

    Sample origin and environmental data

    Location and sample typeSampleCore depth (cm)Water depth (m)Coordinates (°N, °W)Description
    Eel RiverT2014-755040.48, 124.36Clam patch, high CH4 fosmid library
    GZfos
    Monterey Canyon
        SeepF17.10-2595536.77, 122.08Clam patch, high CH4
        NonseepC4.1AMIS microcosma
    Blake RidgePC26762,70731.53, 75.45Hemipelagic sediment
    • ↵ a AMIS microcosm cultured from nonseep reference core collected at least 25 m away from any known seep site.

  • TABLE 2.

    Archaeal 16s rDNA and mcrA clone recovery from MOA-containing sediments and fosmid DNA librarya

    DNAGroupRecovery (no. of clones)Total no. of clones
    Eel RiverMonterey Canyon F17.1AMIS microcosm C4.1Blake Ridge PC26
    T201Gzfos
    Archaeal 16s rDNAANME-16281374
    ANME-2
    ANME-2a14142
    ANME-2b99
    ANME-2c201274391
    Methanogen-like112224
    Other64931591
    mcrA groupa13492551
    b+6+ND6
    c34314529
    d134
    e33
    • ↵ a T201 environmental sequences and the Gzfos library were both derived from the same purified cell preparation of MOA from Eel River T201 sediment (see text). Environmental samples and fosmid library were screened with universal mcrA primers ME-1 and ME-2 and ANME-1 type b-specific mcrA primers AOM39 and AOM40 (see text). +, positive amplification with AOM39 and AOM40 primer set. mcrA group represents conceptual translation product. ND, not determined.

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Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea
Steven J. Hallam, Peter R. Girguis, Christina M. Preston, Paul M. Richardson, Edward F. DeLong
Applied and Environmental Microbiology Sep 2003, 69 (9) 5483-5491; DOI: 10.1128/AEM.69.9.5483-5491.2003

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Identification of Methyl Coenzyme M Reductase A (mcrA) Genes Associated with Methane-Oxidizing Archaea
Steven J. Hallam, Peter R. Girguis, Christina M. Preston, Paul M. Richardson, Edward F. DeLong
Applied and Environmental Microbiology Sep 2003, 69 (9) 5483-5491; DOI: 10.1128/AEM.69.9.5483-5491.2003
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KEYWORDS

Archaea
methane
Oxidoreductases

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