Limits...
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: The associated microbial communities were mainly composed of bacteria, most of which seemed heterotrophic, whereas archaea were negligible.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

Relative abundance of 16S/18S rRNA gene sequences affiliated to lineages displaying metabolisms favoring carbonate precipitation in Alchichica microbialites. Sizes of pie charts (and the values within brackets) indicate the total proportion represented by these sequences compared to the total number of rRNA gene sequences in each sample. Chloroplasts are not included (to see the proportion of photosynthetic eukaryotes based on chloroplast sequences see Supplementary Figure S4).
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4525015&req=5

Figure 4: Relative abundance of 16S/18S rRNA gene sequences affiliated to lineages displaying metabolisms favoring carbonate precipitation in Alchichica microbialites. Sizes of pie charts (and the values within brackets) indicate the total proportion represented by these sequences compared to the total number of rRNA gene sequences in each sample. Chloroplasts are not included (to see the proportion of photosynthetic eukaryotes based on chloroplast sequences see Supplementary Figure S4).

Mentions: Between 15 and 35% of the total number of 16S/18S rRNA gene sequences in each metagenome corresponded to lineages potentially promoting carbonate precipitation, most of them corresponding to oxygenic or anoxygenic photosynthesizers (Figure 4). This implies that the remaining rRNA gene sequences (between ca. 65 and 85% of the total) corresponded to non-photosynthetic organisms, most of which are likely heterotrophs carrying out aerobic or anaerobic respiration or fermentation. Their metabolic activity would tend to counterbalance the carbonate-promoting action of photosynthesis and sulfate reduction (Dupraz and Visscher, 2005). Consequently, for net carbonate precipitation to occur, photosynthesis and/or sulfate reduction must be more active than respiration and/or the hydrochemical conditions override the acidification resulting from respiration and fermentation. Interestingly, although the proportion of cyanobacterial sequences was abundant and even dominated in AL-N samples, between roughly 25% and up to almost 70% of the carbonate biomineralization potential corresponded to others groups. Notably, although the total relative proportion of all eukaryotic rDNA sequences represented from 2 to 15% at most (Figure 3A), photosynthetic eukaryotes accounted for higher proportions among the organisms with carbonate precipitation potential, reaching up values of 20 to 50% in some samples (respectively, AL-N-10 and especially the diatom-dominated AL-W metagenome; Figure 4). Although anoxygenic photosynthesizers varied, they reached similar relatively high (∼15%) proportions in AL-W and all AL-N samples but AL-N-15, where they were less abundant. Finally, sulfate reduction, although relatively minor in all the microbialite fragments analyzed, was relatively abundant in AL-N-1, ca. 20%. The higher proportion of 16S rRNA genes affiliated to anoxygenic phototrophs and sulfate reducers in this sample might in principle suggest that the sampled microbialite fragment (or the mineral grains that we detached from all over the surface for the analysis, see Materials and Methods) contained larger portion of anoxic zones than the other microbialite fragments. However, there might be alternative or additional explanations not related to global anoxia, since typically anaerobic sulfate reducers have been conspicuously observed to be abundant and very active in oxic areas of microbial mats (e.g., Teske et al., 1998; Minz et al., 1999). Also, anoxygenic phototrophs can establish symbioses within sheaths of filamentous cyanobacteria belonging to the Oscillatoriales (D’Amelio et al., 1987). Coincidentally, members of the Oscillatoriales are the dominant cyanobacteria in the AL-N-1 microbialite fragment. Finally, it might also be that the collected fragment (or part of it) was placed in a relatively shadowed area, and this particular situation might have selected for anoxygenic phototrophs, which are adapted to lower light intensities. At any rate, this observation indicates that the microbial communities vary within small spatial scales in response to the heterogeneous local physico-chemical conditions. It also suggests that anoxygenic photosynthesis and sulfate-reduction can be responsible for an important fraction of carbonate precipitation in relatively oxygen-poor microbialite zones, making them potentially interesting areas to study as analogs of stromatolites formed in the Precambrian before oxygen levels significantly raised (Bosak et al., 2007; Farquhar et al., 2011).


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)

Relative abundance of 16S/18S rRNA gene sequences affiliated to lineages displaying metabolisms favoring carbonate precipitation in Alchichica microbialites. Sizes of pie charts (and the values within brackets) indicate the total proportion represented by these sequences compared to the total number of rRNA gene sequences in each sample. Chloroplasts are not included (to see the proportion of photosynthetic eukaryotes based on chloroplast sequences see Supplementary Figure S4).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 4: Relative abundance of 16S/18S rRNA gene sequences affiliated to lineages displaying metabolisms favoring carbonate precipitation in Alchichica microbialites. Sizes of pie charts (and the values within brackets) indicate the total proportion represented by these sequences compared to the total number of rRNA gene sequences in each sample. Chloroplasts are not included (to see the proportion of photosynthetic eukaryotes based on chloroplast sequences see Supplementary Figure S4).
Mentions: Between 15 and 35% of the total number of 16S/18S rRNA gene sequences in each metagenome corresponded to lineages potentially promoting carbonate precipitation, most of them corresponding to oxygenic or anoxygenic photosynthesizers (Figure 4). This implies that the remaining rRNA gene sequences (between ca. 65 and 85% of the total) corresponded to non-photosynthetic organisms, most of which are likely heterotrophs carrying out aerobic or anaerobic respiration or fermentation. Their metabolic activity would tend to counterbalance the carbonate-promoting action of photosynthesis and sulfate reduction (Dupraz and Visscher, 2005). Consequently, for net carbonate precipitation to occur, photosynthesis and/or sulfate reduction must be more active than respiration and/or the hydrochemical conditions override the acidification resulting from respiration and fermentation. Interestingly, although the proportion of cyanobacterial sequences was abundant and even dominated in AL-N samples, between roughly 25% and up to almost 70% of the carbonate biomineralization potential corresponded to others groups. Notably, although the total relative proportion of all eukaryotic rDNA sequences represented from 2 to 15% at most (Figure 3A), photosynthetic eukaryotes accounted for higher proportions among the organisms with carbonate precipitation potential, reaching up values of 20 to 50% in some samples (respectively, AL-N-10 and especially the diatom-dominated AL-W metagenome; Figure 4). Although anoxygenic photosynthesizers varied, they reached similar relatively high (∼15%) proportions in AL-W and all AL-N samples but AL-N-15, where they were less abundant. Finally, sulfate reduction, although relatively minor in all the microbialite fragments analyzed, was relatively abundant in AL-N-1, ca. 20%. The higher proportion of 16S rRNA genes affiliated to anoxygenic phototrophs and sulfate reducers in this sample might in principle suggest that the sampled microbialite fragment (or the mineral grains that we detached from all over the surface for the analysis, see Materials and Methods) contained larger portion of anoxic zones than the other microbialite fragments. However, there might be alternative or additional explanations not related to global anoxia, since typically anaerobic sulfate reducers have been conspicuously observed to be abundant and very active in oxic areas of microbial mats (e.g., Teske et al., 1998; Minz et al., 1999). Also, anoxygenic phototrophs can establish symbioses within sheaths of filamentous cyanobacteria belonging to the Oscillatoriales (D’Amelio et al., 1987). Coincidentally, members of the Oscillatoriales are the dominant cyanobacteria in the AL-N-1 microbialite fragment. Finally, it might also be that the collected fragment (or part of it) was placed in a relatively shadowed area, and this particular situation might have selected for anoxygenic phototrophs, which are adapted to lower light intensities. At any rate, this observation indicates that the microbial communities vary within small spatial scales in response to the heterogeneous local physico-chemical conditions. It also suggests that anoxygenic photosynthesis and sulfate-reduction can be responsible for an important fraction of carbonate precipitation in relatively oxygen-poor microbialite zones, making them potentially interesting areas to study as analogs of stromatolites formed in the Precambrian before oxygen levels significantly raised (Bosak et al., 2007; Farquhar et al., 2011).

Bottom Line: The associated microbial communities were mainly composed of bacteria, most of which seemed heterotrophic, whereas archaea were negligible.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