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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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16S rRNA tree indicating the possibility of a candidate class that includes Iplasma.Ferroplasma acidarmanus is Fer1 and Fer2. Bootstrap values are shown at branch splits. Gene start and stop positions and Genbank accession numbers are listed after organism names.
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Figure 1: 16S rRNA tree indicating the possibility of a candidate class that includes Iplasma.Ferroplasma acidarmanus is Fer1 and Fer2. Bootstrap values are shown at branch splits. Gene start and stop positions and Genbank accession numbers are listed after organism names.

Mentions: We previously published a phylogenetic tree of the 16S rRNA gene of the AMD plasmas [16,17]. Here we improve upon that tree with the addition of a number of new taxa. This tree illustrates that the Richmond Mine AMD plasmas form the following clades: A-, B-, and Cplasma, E- with G-plasma, Dplasma with a number of environmental clones, I-plasma with a number of environmental clones, and the Ferroplasma spp. with Acidiplasma aeolicum. All of the 16S rRNA gene sequences, other than those of Fer1 and Fer2 (which have identical sequences), share less than 97% nucleotide identity. The Iplasma gene is the most divergent, and it is almost certainly not a member of the order Thermoplasmatales or the class Thermoplasmata (Figure 1, Additional file 1, Additional file 2). We found evidence for this classification in the phylogenetic analysis for both 16S rRNA and ribosomal protein S15 genes, where Iplasma groups outside of the Thermoplasmata clade (Figure 1 and Additional file 3) as observed previously [16,17,19,20]. In the case of the 16S tree, Iplasma forms a monophyletic group with a number of environmental clones from acidic solfataric mud and acidic springs (Genbank) [21]. Because archaeal phylogeny is still unresolved, it is impossible to exactly determine the phylogeny of new taxa [22]. However, the branch length separating Iplasma and the Thermoplasmata organisms is greater than 0.25, supporting the separation of Iplasma into a new class of Euryarchaea. We previously suggested this in Justice et al., 2012 [20], but the current study provides much more extensive evidence for this classification. The monophyletic clustering of Eplasma and Gplasma and that of A-, B-, and C-, and Dplasma on the 16S rRNA tree suggests that they belong to new genera of Thermoplasmatales (Figure 1, Additional files 1, 2). This finding is further supported by similar amino acid identities of shared orthologs from A-, E-, and Gplasma to the other Thermoplasmatales archaea (Additional file 4).


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)

16S rRNA tree indicating the possibility of a candidate class that includes Iplasma.Ferroplasma acidarmanus is Fer1 and Fer2. Bootstrap values are shown at branch splits. Gene start and stop positions and Genbank accession numbers are listed after organism names.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: 16S rRNA tree indicating the possibility of a candidate class that includes Iplasma.Ferroplasma acidarmanus is Fer1 and Fer2. Bootstrap values are shown at branch splits. Gene start and stop positions and Genbank accession numbers are listed after organism names.
Mentions: We previously published a phylogenetic tree of the 16S rRNA gene of the AMD plasmas [16,17]. Here we improve upon that tree with the addition of a number of new taxa. This tree illustrates that the Richmond Mine AMD plasmas form the following clades: A-, B-, and Cplasma, E- with G-plasma, Dplasma with a number of environmental clones, I-plasma with a number of environmental clones, and the Ferroplasma spp. with Acidiplasma aeolicum. All of the 16S rRNA gene sequences, other than those of Fer1 and Fer2 (which have identical sequences), share less than 97% nucleotide identity. The Iplasma gene is the most divergent, and it is almost certainly not a member of the order Thermoplasmatales or the class Thermoplasmata (Figure 1, Additional file 1, Additional file 2). We found evidence for this classification in the phylogenetic analysis for both 16S rRNA and ribosomal protein S15 genes, where Iplasma groups outside of the Thermoplasmata clade (Figure 1 and Additional file 3) as observed previously [16,17,19,20]. In the case of the 16S tree, Iplasma forms a monophyletic group with a number of environmental clones from acidic solfataric mud and acidic springs (Genbank) [21]. Because archaeal phylogeny is still unresolved, it is impossible to exactly determine the phylogeny of new taxa [22]. However, the branch length separating Iplasma and the Thermoplasmata organisms is greater than 0.25, supporting the separation of Iplasma into a new class of Euryarchaea. We previously suggested this in Justice et al., 2012 [20], but the current study provides much more extensive evidence for this classification. The monophyletic clustering of Eplasma and Gplasma and that of A-, B-, and C-, and Dplasma on the 16S rRNA tree suggests that they belong to new genera of Thermoplasmatales (Figure 1, Additional files 1, 2). This finding is further supported by similar amino acid identities of shared orthologs from A-, E-, and Gplasma to the other Thermoplasmatales archaea (Additional file 4).

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