An Early-Branching Microbialite Cyanobacterium Forms Intracellular Carbonates

Couradeau, Estelle; Benzerara, Karim; Gérard, Emmanuelle; Moreira, David; Bernard, Sylvain; Brown, Gordon E.; López‐García, Purificación

doi:10.1126/science.1216171

Cited by 212 publications

(225 citation statements)

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“…One striking observation is that aragonite appears recurrently associated with one predominant type of cyanobacteria having the typical morphology of Pleurocapsales (Figures 4-6 and Supplementary Figures S3, S4 and S5). So far, few studies have suggested that some species could be specifically associated with mineral precipitation within the complex diversity of a biofilm (for example, Planavsky et al, 2009, Couradeau et al, 2012. Here we show that a specific lineage of cyanobacteria can orient carbonate precipitation towards aragonite, whereas hydromagnesite precipitates elsewhere.…”

Section: Discussionmentioning

confidence: 71%

“…Under these conditions, the precipitation of hydromagnesite (Mg 5 (CO 3 )4(OH)2 þ 4H 2 O), which is the dominant carbonate mineral in microbialites, is naturally favored (Kaźmierczak et al, 2011). Alchichica microbialites harbor a wide diversity of cyanobacteria, among which members of the Oscillatoriales and Pleurocapsales are the most abundant, but also members of many other prokaryotic and eukaryotic lineages are present (Couradeau et al, 2011(Couradeau et al, , 2012.…”

Section: Introductionmentioning

confidence: 99%

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Specific carbonate–microbe interactions in the modern microbialites of Lake Alchichica (Mexico)

et al. 2013

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The role of microorganisms in microbialite formation remains unresolved: do they induce mineral precipitation (microbes first) or do they colonize and/or entrap abiotic mineral precipitates (minerals first)? Does this role vary from one species to another? And what is the impact of mineral precipitation on microbial ecology? To explore potential biogenic carbonate precipitation, we studied cyanobacteria–carbonate assemblages in modern hydromagnesite-dominated microbialites from the alkaline Lake Alchichica (Mexico), by coupling three-dimensional imaging of molecular fluorescence emitted by microorganisms, using confocal laser scanning microscopy, and Raman scattering/spectrometry from the associated minerals at a microscale level. Both hydromagnesite and aragonite precipitate within a complex biofilm composed of photosynthetic and other microorganisms. Morphology and pigment-content analysis of dominant photosynthetic microorganisms revealed up to six different cyanobacterial morphotypes belonging to Oscillatoriales, Chroococcales, Nostocales and Pleurocapsales, as well as several diatoms and other eukaryotic microalgae. Interestingly, one of these morphotypes, Pleurocapsa-like, appeared specifically associated with aragonite minerals, the oldest parts of actively growing Pleurocapsa-like colonies being always aragonite-encrusted. We hypothesize that actively growing cells of Pleurocapsales modify local environmental conditions favoring aragonite precipitation at the expense of hydromagnesite, which precipitates at seemingly random locations within the biofilm. Therefore, at least part of the mineral precipitation in Alchichica microbialites is most likely biogenic and the type of biominerals formed depends on the nature of the phylogenetic lineage involved. This observation may provide clues to identify lineage-specific biosignatures in fossil stromatolites from modern to Precambrian times.

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Section: Discussionmentioning

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Specific carbonate–microbe interactions in the modern microbialites of Lake Alchichica (Mexico)

et al. 2013

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“…Their most conspicuous characteristic is the accumulation of numerous large inclusions filling the majority of the cell that were first described as calcium oxalate, giving the type species Achromatium oxaliferum its name, but which were later recognized as colloidal calcite (West and Griffiths, 1913;Bersa, 1920;Head et al, 1996). Recently, cyanobacteria (Gloeobacterales) were found to form amorphous calcium-magnesium-strontium-barium carbonate inclusions (Couradeau et al, 2012); however, the massive accumulation of CaCO 3 in Achromatium is still a unique peculiarity in the microbial world (Head et al, 2000;Gray and Head, 2014). The biological function of internal calcite is under investigation, and hypotheses include its usage as buffer, a source of CO 2 or a mechanism of buoyancy regulation (Gray, 2006, reviewed in Head et al, 2000.…”

Section: Introductionmentioning

confidence: 99%

Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh

et al. 2015

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Large sulfur bacteria of the genus Achromatium are exceptional among Bacteria and Archaea as they can accumulate high amounts of internal calcite. Although known for more than 100 years, they remain uncultured, and only freshwater populations have been studied so far. Here we investigate a marine population of calcite-accumulating bacteria that is primarily found at the sediment surface of tide pools in a salt marsh, where high sulfide concentrations meet oversaturated oxygen concentrations during the day. Dynamic sulfur cycling by phototrophic sulfide-oxidizing and heterotrophic sulfate-reducing bacteria co-occurring in these sediments creates a highly sulfidic environment that we propose induces behavioral differences in the Achromatium population compared with reported migration patterns in a low-sulfide environment. Fluctuating intracellular calcium/sulfur ratios at different depths and times of day indicate a biochemical reaction of the salt marsh Achromatium to diurnal changes in sedimentary redox conditions. We correlate this calcite dynamic with new evidence regarding its formation/mobilization and suggest general implications as well as a possible biological function of calcite accumulation in large bacteria in the sediment environment that is governed by gradients. Finally, we propose a new taxonomic classification of the salt marsh Achromatium based on their adaptation to a significantly different habitat than their freshwater relatives, as indicated by their differential behavior as well as phylogenetic distance on 16S ribosomal RNA gene level. In future studies, whole-genome characterization and additional ecophysiological factors could further support the distinctive position of salt marsh Achromatium.

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“…A late emerging violet clade is consistent with the inclusion of Synechococcus sp. JA-2-3B′A and JA-3-3AB in the order Gloeobacterales based on sequences from a recently cultured early branching cyanobacteria (26). #sp., number of genomes.…”

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Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

Szöllősi

Boussau

Abby

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

150

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The timing of the evolution of microbial life has largely remained elusive due to the scarcity of prokaryotic fossil record and the confounding effects of the exchange of genes among possibly distant species. The history of gene transfer events, however, is not a series of individual oddities; it records which lineages were concurrent and thus provides information on the timing of species diversification. Here, we use a probabilistic model of genome evolution that accounts for differences between gene phylogenies and the species tree as series of duplication, transfer, and loss events to reconstruct chronologically ordered species phylogenies. Using simulations we show that we can robustly recover accurate chronologically ordered species phylogenies in the presence of gene tree reconstruction errors and realistic rates of duplication, transfer, and loss. Using genomic data we demonstrate that we can infer rooted species phylogenies using homologous gene families from complete genomes of 10 bacterial and archaeal groups. Focusing on cyanobacteria, distinguished among prokaryotes by a relative abundance of fossils, we infer the maximum likelihood chronologically ordered species phylogeny based on 36 genomes with 8,332 homologous gene families. We find the order of speciation events to be in full agreement with the fossil record and the inferred phylogeny of cyanobacteria to be consistent with the phylogeny recovered from established phylogenomics methods. Our results demonstrate that lateral gene transfers, detected by probabilistic models of genome evolution, can be used as a source of information on the timing of evolution, providing a valuable complement to the limited prokaryotic fossil record. molecular dating | gene tree reconciliation | birth-death model A central aspect of Earth's history is the pattern and timing of diversification of the species that inhabit it. In macroorganisms such as animals or plants, an abundant fossil record, the accumulation of genomic data, and the development of models of molecular evolution accommodating for varying rates of evolutionary changes among lineages are progressively yielding an intelligible picture (1-4). In contrast, the dating of the evolution of microbial life remains largely elusive (5, 6). This situation results from the convergence of two main factors: first, fossils, especially bacterial and archaeal ones, are scarce or cannot be traced to a specific lineage. Therefore, any inference of the timing of microbial evolution must rely almost exclusively on molecular data constrained only by a handful of dates during the course of more than three billion years of evolution. Second, molecular data can be difficult to interpret in terms of patterns of species diversification. Lateral gene transfers (LGTs), the exchange of genes among possibly distant species, have tangled gene phylogenies to the extent that they provide a deeply blurred view of the relationships between lineages. Different approaches [e.g., concatenation, supertrees (7, 8)] have been proposed to ove...

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An Early-Branching Microbialite Cyanobacterium Forms Intracellular Carbonates

Cited by 212 publications

References 35 publications

Specific carbonate–microbe interactions in the modern microbialites of Lake Alchichica (Mexico)

Specific carbonate–microbe interactions in the modern microbialites of Lake Alchichica (Mexico)

Calcite-accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh

Phylogenetic modeling of lateral gene transfer reconstructs the pattern and relative timing of speciations

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