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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.

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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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Cryo-electron microscopy of AMD plasma cells with putative pili. Panel A and panel B show evidence of pili on two different cells collected from the Richmond Mine AMD. Arrows point to pili. Vesicle-like structures are delineated by a single membrane layer around an ovoid shape in each cell’s cytoplasm.
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Figure 5: Cryo-electron microscopy of AMD plasma cells with putative pili. Panel A and panel B show evidence of pili on two different cells collected from the Richmond Mine AMD. Arrows point to pili. Vesicle-like structures are delineated by a single membrane layer around an ovoid shape in each cell’s cytoplasm.

Mentions: In addition to flagellar assembly genes, a number of the AMD plasma genomes contain genes for Type II secretion or Type IV pili that are used in twitching motility or possibly conjugation or attachment to the biofilm or other surfaces. All of the genomes except for Fer1 and Fer2 contain some of these genes, and in Eplasma, Gplasma, and Iplasma they are in a cluster with conserved gene order among the AMD plasmas (Additional file 23). Cryo-EM confirms the existence of pili, and shows attachment of the pili from the original cell to other cells (Figure 5, Additional file 24).


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)

Cryo-electron microscopy of AMD plasma cells with putative pili. Panel A and panel B show evidence of pili on two different cells collected from the Richmond Mine AMD. Arrows point to pili. Vesicle-like structures are delineated by a single membrane layer around an ovoid shape in each cell’s cytoplasm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Cryo-electron microscopy of AMD plasma cells with putative pili. Panel A and panel B show evidence of pili on two different cells collected from the Richmond Mine AMD. Arrows point to pili. Vesicle-like structures are delineated by a single membrane layer around an ovoid shape in each cell’s cytoplasm.
Mentions: In addition to flagellar assembly genes, a number of the AMD plasma genomes contain genes for Type II secretion or Type IV pili that are used in twitching motility or possibly conjugation or attachment to the biofilm or other surfaces. All of the genomes except for Fer1 and Fer2 contain some of these genes, and in Eplasma, Gplasma, and Iplasma they are in a cluster with conserved gene order among the AMD plasmas (Additional file 23). Cryo-EM confirms the existence of pili, and shows attachment of the pili from the original cell to other cells (Figure 5, Additional file 24).

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