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Metagenome-based diversity analyses suggest a significant contribution of non-cyanobacterial lineages to carbonate precipitation in modern microbialites.

Saghaï A, Zivanovic Y, Zeyen N, Moreira D, Benzerara K, Deschamps P, Bertolino P, Ragon M, Tavera R, López-Archilla AI, López-García P - Front Microbiol (2015)

Bottom Line: Cyanobacteria are thought to play a key role in carbonate formation due to their metabolic activity, but other organisms carrying out oxygenic photosynthesis (photosynthetic eukaryotes) or other metabolisms (e.g., anoxygenic photosynthesis, sulfate reduction), may also contribute to carbonate formation.Although cyanobacteria were the most important bacterial group contributing to the carbonate precipitation potential, photosynthetic eukaryotes, anoxygenic photosynthesizers and sulfate reducers were also very abundant.Despite the previous identification of intracellularly calcifying cyanobacteria in Alchichica microbialites, most carbonate precipitation seems extracellular in this system.

View Article: PubMed Central - PubMed

Affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud Orsay, France.

ABSTRACT
Cyanobacteria are thought to play a key role in carbonate formation due to their metabolic activity, but other organisms carrying out oxygenic photosynthesis (photosynthetic eukaryotes) or other metabolisms (e.g., anoxygenic photosynthesis, sulfate reduction), may also contribute to carbonate formation. To obtain more quantitative information than that provided by more classical PCR-dependent methods, we studied the microbial diversity of microbialites from the Alchichica crater lake (Mexico) by mining for 16S/18S rRNA genes in metagenomes obtained by direct sequencing of environmental DNA. We studied samples collected at the Western (AL-W) and Northern (AL-N) shores of the lake and, at the latter site, along a depth gradient (1, 5, 10, and 15 m depth). The associated microbial communities were mainly composed of bacteria, most of which seemed heterotrophic, whereas archaea were negligible. Eukaryotes composed a relatively minor fraction dominated by photosynthetic lineages, diatoms in AL-W, influenced by Si-rich seepage waters, and green algae in AL-N samples. Members of the Gammaproteobacteria and Alphaproteobacteria classes of Proteobacteria, Cyanobacteria, and Bacteroidetes were the most abundant bacterial taxa, followed by Planctomycetes, Deltaproteobacteria (Proteobacteria), Verrucomicrobia, Actinobacteria, Firmicutes, and Chloroflexi. Community composition varied among sites and with depth. Although cyanobacteria were the most important bacterial group contributing to the carbonate precipitation potential, photosynthetic eukaryotes, anoxygenic photosynthesizers and sulfate reducers were also very abundant. Cyanobacteria affiliated to Pleurocapsales largely increased with depth. Scanning electron microscopy (SEM) observations showed considerable areas of aragonite-encrusted Pleurocapsa-like cyanobacteria at microscale. Multivariate statistical analyses showed a strong positive correlation of Pleurocapsales and Chroococcales with aragonite formation at macroscale, and suggest a potential causal link. Despite the previous identification of intracellularly calcifying cyanobacteria in Alchichica microbialites, most carbonate precipitation seems extracellular in this system.

No MeSH data available.


Related in: MedlinePlus

Histograms showing the relative abundance of 16S/18S rRNA gene sequences in Alchichica microbialite metagenomes assigned to major different high-rank taxa. (A) Proportion of sequences assigned to the three domains of life: archaea, bacteria and eukaryotes to the exclusions of metazoans (see also Supplementary Figure S1). (B) Phylogenetic clades of microbial eukaryotes, (C) bacterial phyla or classes (for the Proteobacteria), and (D) cyanobacterial orders. Neither singletons nor chloroplasts were included (their proportions are shown in Supplementary Figures S2–S4).
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Figure 3: Histograms showing the relative abundance of 16S/18S rRNA gene sequences in Alchichica microbialite metagenomes assigned to major different high-rank taxa. (A) Proportion of sequences assigned to the three domains of life: archaea, bacteria and eukaryotes to the exclusions of metazoans (see also Supplementary Figure S1). (B) Phylogenetic clades of microbial eukaryotes, (C) bacterial phyla or classes (for the Proteobacteria), and (D) cyanobacterial orders. Neither singletons nor chloroplasts were included (their proportions are shown in Supplementary Figures S2–S4).

Mentions: In order to get a more accurate taxonomic affiliation of the most abundant sequences in our datasets, we first clustered sequences that were 100% identical along their whole length (see Materials and Methods). We then chose the longest sequence as representative of the whole cluster and BLAST it against public databases to get a more accurate taxonomic affiliation of the cluster. However, for subsequent quantitative analysis, only the number of individual sequences was taken into account. Individual sequences that did not match any other sequence in each of our metagenomic datasets were analyzed independently. In the following, we refer to these unique sequences as ‘singletons’ by analogy with unique amplified sequences in amplicon studies. However, contrary to singletons in amplicon studies, a portion of which corresponds to sequencing artifacts or PCR chimeras, metagenomic singletons are unlikely to be artifacts and likely reflect lower abundances of the corresponding taxa. Metagenomic singletons accounted for ca. 5–15% of the predicted 16S/18S rRNA genes in our datasets (Table 2). Comparing the phylogenetic affiliation and relative abundance of clustered sequences and singletons should reveal if patterns of phylogenetic diversity differed significantly between high and low abundant organisms. However, the distribution of relative proportions of singletons and of more abundant sequences among major bacterial and eukaryotic taxa were remarkably similar (compare Figure 3 and Supplementary Figure S2). This suggests, with minor exceptions (see below), that low-abundant organisms essentially correspond to low-abundance species or genera within the same dominant high-rank taxa (orders or phyla), and not to the occurrence of novel or rare divergent taxa.


Metagenome-based diversity analyses suggest a significant contribution of non-cyanobacterial lineages to carbonate precipitation in modern microbialites.

Saghaï A, Zivanovic Y, Zeyen N, Moreira D, Benzerara K, Deschamps P, Bertolino P, Ragon M, Tavera R, López-Archilla AI, López-García P - Front Microbiol (2015)

Histograms showing the relative abundance of 16S/18S rRNA gene sequences in Alchichica microbialite metagenomes assigned to major different high-rank taxa. (A) Proportion of sequences assigned to the three domains of life: archaea, bacteria and eukaryotes to the exclusions of metazoans (see also Supplementary Figure S1). (B) Phylogenetic clades of microbial eukaryotes, (C) bacterial phyla or classes (for the Proteobacteria), and (D) cyanobacterial orders. Neither singletons nor chloroplasts were included (their proportions are shown in Supplementary Figures S2–S4).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4525015&req=5

Figure 3: Histograms showing the relative abundance of 16S/18S rRNA gene sequences in Alchichica microbialite metagenomes assigned to major different high-rank taxa. (A) Proportion of sequences assigned to the three domains of life: archaea, bacteria and eukaryotes to the exclusions of metazoans (see also Supplementary Figure S1). (B) Phylogenetic clades of microbial eukaryotes, (C) bacterial phyla or classes (for the Proteobacteria), and (D) cyanobacterial orders. Neither singletons nor chloroplasts were included (their proportions are shown in Supplementary Figures S2–S4).
Mentions: In order to get a more accurate taxonomic affiliation of the most abundant sequences in our datasets, we first clustered sequences that were 100% identical along their whole length (see Materials and Methods). We then chose the longest sequence as representative of the whole cluster and BLAST it against public databases to get a more accurate taxonomic affiliation of the cluster. However, for subsequent quantitative analysis, only the number of individual sequences was taken into account. Individual sequences that did not match any other sequence in each of our metagenomic datasets were analyzed independently. In the following, we refer to these unique sequences as ‘singletons’ by analogy with unique amplified sequences in amplicon studies. However, contrary to singletons in amplicon studies, a portion of which corresponds to sequencing artifacts or PCR chimeras, metagenomic singletons are unlikely to be artifacts and likely reflect lower abundances of the corresponding taxa. Metagenomic singletons accounted for ca. 5–15% of the predicted 16S/18S rRNA genes in our datasets (Table 2). Comparing the phylogenetic affiliation and relative abundance of clustered sequences and singletons should reveal if patterns of phylogenetic diversity differed significantly between high and low abundant organisms. However, the distribution of relative proportions of singletons and of more abundant sequences among major bacterial and eukaryotic taxa were remarkably similar (compare Figure 3 and Supplementary Figure S2). This suggests, with minor exceptions (see below), that low-abundant organisms essentially correspond to low-abundance species or genera within the same dominant high-rank taxa (orders or phyla), and not to the occurrence of novel or rare divergent taxa.

Bottom Line: Cyanobacteria are thought to play a key role in carbonate formation due to their metabolic activity, but other organisms carrying out oxygenic photosynthesis (photosynthetic eukaryotes) or other metabolisms (e.g., anoxygenic photosynthesis, sulfate reduction), may also contribute to carbonate formation.Although cyanobacteria were the most important bacterial group contributing to the carbonate precipitation potential, photosynthetic eukaryotes, anoxygenic photosynthesizers and sulfate reducers were also very abundant.Despite the previous identification of intracellularly calcifying cyanobacteria in Alchichica microbialites, most carbonate precipitation seems extracellular in this system.

View Article: PubMed Central - PubMed

Affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud Orsay, France.

ABSTRACT
Cyanobacteria are thought to play a key role in carbonate formation due to their metabolic activity, but other organisms carrying out oxygenic photosynthesis (photosynthetic eukaryotes) or other metabolisms (e.g., anoxygenic photosynthesis, sulfate reduction), may also contribute to carbonate formation. To obtain more quantitative information than that provided by more classical PCR-dependent methods, we studied the microbial diversity of microbialites from the Alchichica crater lake (Mexico) by mining for 16S/18S rRNA genes in metagenomes obtained by direct sequencing of environmental DNA. We studied samples collected at the Western (AL-W) and Northern (AL-N) shores of the lake and, at the latter site, along a depth gradient (1, 5, 10, and 15 m depth). The associated microbial communities were mainly composed of bacteria, most of which seemed heterotrophic, whereas archaea were negligible. Eukaryotes composed a relatively minor fraction dominated by photosynthetic lineages, diatoms in AL-W, influenced by Si-rich seepage waters, and green algae in AL-N samples. Members of the Gammaproteobacteria and Alphaproteobacteria classes of Proteobacteria, Cyanobacteria, and Bacteroidetes were the most abundant bacterial taxa, followed by Planctomycetes, Deltaproteobacteria (Proteobacteria), Verrucomicrobia, Actinobacteria, Firmicutes, and Chloroflexi. Community composition varied among sites and with depth. Although cyanobacteria were the most important bacterial group contributing to the carbonate precipitation potential, photosynthetic eukaryotes, anoxygenic photosynthesizers and sulfate reducers were also very abundant. Cyanobacteria affiliated to Pleurocapsales largely increased with depth. Scanning electron microscopy (SEM) observations showed considerable areas of aragonite-encrusted Pleurocapsa-like cyanobacteria at microscale. Multivariate statistical analyses showed a strong positive correlation of Pleurocapsales and Chroococcales with aragonite formation at macroscale, and suggest a potential causal link. Despite the previous identification of intracellularly calcifying cyanobacteria in Alchichica microbialites, most carbonate precipitation seems extracellular in this system.

No MeSH data available.


Related in: MedlinePlus