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Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea.

Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC, Banfield JF - BMC Genomics (2013)

Bottom Line: These results greatly expand genomic information available for this archaeal order.These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence.Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720, USA.

ABSTRACT

Background: Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order.

Results: We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis.

Conclusion: The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.

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Cluster of unique genes in Gplasma. Arrows are proportional to the length of each gene and indicate its direction of transcription. The gene numbers are shown inside the arrows. All genes are from contig number 13327. Motif and domain-based annotations are shown above the arrows. Genes with no annotations are hypothetical proteins. Rhod indicates a rhodanese-like domain.
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Figure 2: Cluster of unique genes in Gplasma. Arrows are proportional to the length of each gene and indicate its direction of transcription. The gene numbers are shown inside the arrows. All genes are from contig number 13327. Motif and domain-based annotations are shown above the arrows. Genes with no annotations are hypothetical proteins. Rhod indicates a rhodanese-like domain.

Mentions: A genomic island of potential importance was identified in the Gplasma genome. It consists of a block of nine genes that have virtually no orthologs in any of the other Thermoplasmatales genomes and is made up primarily of proteins of unknown function (Figure 2, Additional file 10). All nine of the proteins are represented in a whole community proteomic dataset reported previously [26], and three are among the most highly detected proteins of this organism in that dataset. The motifs and domains identified suggest that a number of these proteins are membrane associated, including a protein containing an AAA + FtsH ATPase domain (gene number 13327_0053) (found in a membrane-integrated metalloprotease [27]), a protein containing six transmembrane motifs and a signal peptide (13327_0056), and another with fourteen transmembrane motifs and a signal peptide (13327_0059). Additionally, three of these proteins include a rhodanese-like domain possibly involved in phosphatase or sulfurtransferase activity and another contains an armadillo repeat region, often used to bind large substrates such as peptides or nucleic acids (13327_0058).


Comparative genomics in acid mine drainage biofilm communities reveals metabolic and structural differentiation of co-occurring archaea.

Yelton AP, Comolli LR, Justice NB, Castelle C, Denef VJ, Thomas BC, Banfield JF - BMC Genomics (2013)

Cluster of unique genes in Gplasma. Arrows are proportional to the length of each gene and indicate its direction of transcription. The gene numbers are shown inside the arrows. All genes are from contig number 13327. Motif and domain-based annotations are shown above the arrows. Genes with no annotations are hypothetical proteins. Rhod indicates a rhodanese-like domain.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750248&req=5

Figure 2: Cluster of unique genes in Gplasma. Arrows are proportional to the length of each gene and indicate its direction of transcription. The gene numbers are shown inside the arrows. All genes are from contig number 13327. Motif and domain-based annotations are shown above the arrows. Genes with no annotations are hypothetical proteins. Rhod indicates a rhodanese-like domain.
Mentions: A genomic island of potential importance was identified in the Gplasma genome. It consists of a block of nine genes that have virtually no orthologs in any of the other Thermoplasmatales genomes and is made up primarily of proteins of unknown function (Figure 2, Additional file 10). All nine of the proteins are represented in a whole community proteomic dataset reported previously [26], and three are among the most highly detected proteins of this organism in that dataset. The motifs and domains identified suggest that a number of these proteins are membrane associated, including a protein containing an AAA + FtsH ATPase domain (gene number 13327_0053) (found in a membrane-integrated metalloprotease [27]), a protein containing six transmembrane motifs and a signal peptide (13327_0056), and another with fourteen transmembrane motifs and a signal peptide (13327_0059). Additionally, three of these proteins include a rhodanese-like domain possibly involved in phosphatase or sulfurtransferase activity and another contains an armadillo repeat region, often used to bind large substrates such as peptides or nucleic acids (13327_0058).

Bottom Line: These results greatly expand genomic information available for this archaeal order.These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence.Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720, USA.

ABSTRACT

Background: Metal sulfide mineral dissolution during bioleaching and acid mine drainage (AMD) formation creates an environment that is inhospitable to most life. Despite dominance by a small number of bacteria, AMD microbial biofilm communities contain a notable variety of coexisting and closely related Euryarchaea, most of which have defied cultivation efforts. For this reason, we used metagenomics to analyze variation in gene content that may contribute to niche differentiation among co-occurring AMD archaea. Our analyses targeted members of the Thermoplasmatales and related archaea. These results greatly expand genomic information available for this archaeal order.

Results: We reconstructed near-complete genomes for uncultivated, relatively low abundance organisms A-, E-, and Gplasma, members of Thermoplasmatales order, and for a novel organism, Iplasma. Genomic analyses of these organisms, as well as Ferroplasma type I and II, reveal that all are facultative aerobic heterotrophs with the ability to use many of the same carbon substrates, including methanol. Most of the genomes share genes for toxic metal resistance and surface-layer production. Only Aplasma and Eplasma have a full suite of flagellar genes whereas all but the Ferroplasma spp. have genes for pili production. Cryogenic-electron microscopy (cryo-EM) and tomography (cryo-ET) strengthen these metagenomics-based ultrastructural predictions. Notably, only Aplasma, Gplasma and the Ferroplasma spp. have predicted iron oxidation genes and Eplasma and Iplasma lack most genes for cobalamin, valine, (iso)leucine and histidine synthesis.

Conclusion: The Thermoplasmatales AMD archaea share a large number of metabolic capabilities. All of the uncultivated organisms studied here (A-, E-, G-, and Iplasma) are metabolically very similar to characterized Ferroplasma spp., differentiating themselves mainly in their genetic capabilities for biosynthesis, motility, and possibly iron oxidation. These results indicate that subtle, but important genomic differences, coupled with unknown differences in gene expression, distinguish these organisms enough to allow for co-existence. Overall this study reveals shared features of organisms from the Thermoplasmatales lineage and provides new insights into the functioning of AMD communities.

Show MeSH
Related in: MedlinePlus