RESUMO
Microbialites are emblematic sedimentary rocks formed by phylogenetically and metabolically complex microbial communities thriving under specific physicochemical conditions. Most microbialites are photosynthesis-based ecosystems frequently formed by carbonates, thereby capturing inorganic carbon in the form of both, organic matter and mineral precipitates. However, little is known about the amount of sequestered carbon and the kinetics of the process, that is, microbialite growth rate. To assess microbialite growth rate and the influence of substrates on carbonate formation in Alchichica, an alkaline crater lake harbouring well-developed carbonate microbialites, we incubated in situ sterilized Nylon mesh, hydromagnesite and aragonite crystals, and bleached-coral aragonite for 2 years. We observed the rapid formation of nascent hydromagnesite and aragonite-containing microbialites on Nylon mesh, with an average growth rate of ~0.6 (and up to 1) mm year-1 . By contrast, only thin (< 0.2 mm) biofilms developed on exposed hydromagnesite and aragonite crystals and bleached-coral aragonite, suggesting decoupled microbial colonization and biomineralization and/or potential interference of those mineral surfaces with new carbonate nucleation. Microbial communities associated with 2-year-old microbialites and biofilms were fully comparable to mature communities populating Lake Alchichica indigenous microbialites.
Assuntos
Lagos , Microbiota , Carbonatos/análise , Carbonatos/química , Sedimentos Geológicos/química , Lagos/química , MéxicoRESUMO
Microbialites are usually carbonate-rich sedimentary rocks formed by the interplay of phylogenetically and metabolically complex microbial communities with their physicochemical environment. Yet, the biotic and abiotic determinants of microbialite formation remain poorly constrained. Here, we analysed the structure of prokaryotic and eukaryotic communities associated with microbialites occurring in several crater lakes of the Trans-Mexican volcanic belt along an alkalinity gradient. Microbialite size and community structure correlated with lake physicochemical parameters, notably alkalinity. Although microbial community composition varied across lake microbialites, major taxa-associated functions appeared quite stable with both, oxygenic and anoxygenic photosynthesis and, to less extent, sulphate reduction, as major putative carbonatogenic processes. Despite interlake microbialite community differences, we identified a microbial core of 247 operational taxonomic units conserved across lake microbialites, suggesting a prominent ecological role in microbialite formation. This core mostly encompassed Cyanobacteria and their typical associated taxa (Bacteroidetes, Planctomycetes) and diverse anoxygenic photosynthetic bacteria, notably Chloroflexi, Alphaproteobacteria (Rhodobacteriales, Rhodospirilalles), Gammaproteobacteria (Chromatiaceae) and minor proportions of Chlorobi. The conserved core represented up to 40% (relative abundance) of the total community in lakes Alchichica and Atexcac, displaying the highest alkalinities and the most conspicuous microbialites. Core microbialite communities associated with carbonatogenesis might be relevant for inorganic carbon sequestration purposes.
Assuntos
Bactérias/metabolismo , Lagos/microbiologia , Microbiota , Bactérias/classificação , Bactérias/genética , Bactérias/isolamento & purificação , Carbonatos/análise , Carbonatos/metabolismo , Eucariotos/classificação , Eucariotos/genética , Eucariotos/isolamento & purificação , Eucariotos/metabolismo , Sedimentos Geológicos/microbiologia , Lagos/química , Lagos/parasitologia , México , FilogeniaRESUMO
Chloroflexales (Chloroflexi) are typical members of the anoxygenic photosynthesizing component of microbial mats and have mostly been characterized from communities associated to hot springs. Here, we report the assembly of five metagenome-assembled genomes (MAGs) of a novel lineage of Chloroflexales found in mesophilic lithifying microbial mats (microbialites) in Lake Alchichica (Mexico). Genomic and phylogenetic analyses revealed that the bins shared 92% of their genes, and these genes were nearly identical despite being assembled from samples collected along a depth gradient (1-15 m depth). We tentatively name this lineage Candidatus Lithoflexus mexicanus. Metabolic predictions based on the MAGs suggest that these chlorosome-lacking mixotrophs share features in central carbon metabolism, electron transport, and adaptations to life under oxic and anoxic conditions, with members of two related lineages, Chloroflexineae and Roseiflexineae. Contrasting with the other diverse microbialite community members, which display much lower genomic conservation along the depth gradient, Ca. L. mexicanus MAGs exhibit remarkable similarity. This might reflect a particular flexibility to acclimate to varying light conditions with depth or the capacity to occupy a very specific spatial ecological niche in microbialites from different depths. Alternatively, Ca. L. mexicanus may also have the ability to modulate its gene expression as a function of the local environmental conditions during diel cycles in microbialites along the depth gradient.
Assuntos
Chloroflexi/genética , Genoma Bacteriano , Lagos/microbiologia , Adaptação Biológica , Anaerobiose , Proteínas de Bactérias , Carotenoides/metabolismo , Chloroflexi/metabolismo , Ecossistema , Transporte de Elétrons , Variação Genética , Metagenoma , México , Consórcios Microbianos , Nitrogênio/metabolismo , Filogenia , Enxofre/metabolismoRESUMO
Modern phototrophic microbial mats are complex communities often used as analogs of major Precambrian ecosystems. Characterizing biotic, notably metabolic, interactions among different microbial mat members is essential to gain insights into the ecology and biogeochemistry of these systems. We applied 16S/18S rRNA metabarcoding approaches to characterize the structure of archaea, bacteria and protist communities from microbial mats collected along strong physicochemical (oxygen, salinity, temperature, depth) gradients in a shallow pond at the salar de Llamara (Chile). All mats were highly diverse, including members of virtually all known high-rank eukaryotic and prokaryotic taxa but also many novel lineages. Bacterial candidate divisions accounted for almost 50% of sequences in deeper mats, while Archaea represented up to 40% of sequences in some mat layers. Molecular phylogenetic analyses revealed six novel deeply divergent archaeal groups, along abundant and diverse Pacearchaeota and Woesearchaeota. Multivariate statistical analyses showed that local environmental conditions strongly influenced community composition. Co-occurrence network structure was markedly different between surface mats located in the oxygenated zone and mats located in transition and anoxic water layers. We identified potential biotic interactions between various high- and low-rank taxa. Notably, a strong positive correlation was observed between Lokiarchaeota and the poorly known candidate bacterial division TA06.
Assuntos
Archaea/classificação , Bactérias/classificação , Biofilmes/classificação , Interações Microbianas/fisiologia , Parasitos/classificação , Lagoas/microbiologia , Animais , Archaea/genética , Bactérias/genética , Biodiversidade , Biofilmes/crescimento & desenvolvimento , Chile , Ecossistema , Parasitos/genética , Processos Fototróficos/fisiologia , Filogenia , RNA Ribossômico 16S/genética , RNA Ribossômico 18S/genética , SalinidadeRESUMO
A unicellular cyanobacterium, strain Alchichica-D10, was isolated from microbialites of the alkaline Lake Alchichica, Mexico. The cells were short rods (3.9±0.6 µm in length and 1.1±0.1 µm in width) forming biofilms of intense emerald green colour. They exhibited red autofluorescence under UV light excitation. UV-visible absorption spectra revealed that they contain chlorophyll a and phycocyanin, and electron microscopy showed the presence of thylakoids. The strain grew within a temperature range of 15-30 °C. Genomic DNA G+C content was 52.2 mol%. The most remarkable feature of this species was its granular cytoplasm, due to the presence of numerous intracellular spherical granules (16-26 per cell) with an average diameter of 270 nm. These granules, easily visible under scanning electron microscopy, were composed of amorphous carbonate containing Ca, Mg, Ba and Sr. A multi-gene phylogeny based on the analysis of 59 conserved protein markers supported robustly that this strain occupies a deep position in the cyanobacterial tree. Based on its phenotypic characters and phylogenetic position, strain Alchichica-D10 is considered to represent a new genus and novel species of cyanobacteria for which the name Gloeomargarita lithophora gen. nov., sp. nov. is proposed. The type strain is Alchichica-D10 (Culture Collection of Algae and Protozoa CCAP strain 1437/1; Collections de Cyanobactéries et Microalgues Vivantes of the Museum National d'Histoire Naturelle in Paris strain PMC 919.15). Furthermore, a new family, Gloeomargaritaceae, and a new order, Gloeoemargaritales, are proposed to accommodate this species under the International Code of Nomenclature for algae, fungi and plants.
Assuntos
Cianobactérias/classificação , Lagos/microbiologia , Filogenia , Técnicas de Tipagem Bacteriana , Composição de Bases , Carbonatos/química , Clorofila/química , Clorofila A , Cianobactérias/genética , Cianobactérias/isolamento & purificação , DNA Bacteriano/genética , México , Ficocianina/química , RNA Ribossômico 16S/genética , Análise de Sequência de DNA , TilacoidesRESUMO
Modern microbialites are often used as analogs of Precambrian stromatolites; therefore, studying the metabolic interplay within their associated microbial communities can help formulating hypotheses on their formation and long-term preservation within the fossil record. We performed a comparative metagenomic analysis of microbialite samples collected at two sites and along a depth gradient in Lake Alchichica (Mexico). The community structure inferred from single-copy gene family identification and long-contig (>10 kb) assignation, consistently with previous rRNA gene surveys, showed a wide prokaryotic diversity dominated by Alphaproteobacteria, Gammaproteobacteria, Cyanobacteria, and Bacteroidetes, while eukaryotes were largely dominated by green algae or diatoms. Functional analyses based on RefSeq, COG and SEED assignations revealed the importance of housekeeping functions, with an overrepresentation of genes involved in carbohydrate metabolism, as compared with other metabolic capacities. The search for genes diagnostic of specific metabolic functions revealed the important involvement of Alphaproteobacteria in anoxygenic photosynthesis and sulfide oxidation, and Cyanobacteria in oxygenic photosynthesis and nitrogen fixation. Surprisingly, sulfate reduction appeared negligible. Comparative analyses suggested functional similarities among various microbial mat and microbialite metagenomes as compared with soil or oceans, but showed differences in microbial processes among microbialite types linked to local environmental conditions.
Assuntos
Alphaproteobacteria/isolamento & purificação , Bacteroidetes/isolamento & purificação , Cianobactérias/isolamento & purificação , Diatomáceas/isolamento & purificação , Gammaproteobacteria/isolamento & purificação , Sedimentos Geológicos/microbiologia , Lagos/microbiologia , Alphaproteobacteria/classificação , Alphaproteobacteria/genética , Bacteroidetes/classificação , Bacteroidetes/genética , Metabolismo dos Carboidratos/genética , Clorófitas/genética , Cianobactérias/classificação , Cianobactérias/genética , Fósseis , Gammaproteobacteria/classificação , Gammaproteobacteria/genética , Metagenoma/genética , Metagenômica/métodos , México , FotossínteseRESUMO
We investigated the morphology and evolutionary relationships of Torodinium spp. and Katodinium glaucum, unarmoured dinoflagellates characterized by a small hyposome. An emended generic description of Torodinium was proposed based on light and scanning electron microscopy. Torodinium exhibited a unique combination of morphological features including a minute hyposome, a long episome with longitudinal ribs and a canal of unknown function on the dextro-lateral side. Unlike any known dinoflagellate both cingulum and sulcus extended in the episome. The apex surface showed ribs that converged in a bill-like projection. The shape of the apical groove was a circular spiral that extended around the apex running in 2.5 turns in an anticlockwise direction. The type species T. teredo was usually longer than T. robustum. The longitudinal outline of T. teredo was linear, with almost parallel margins, a circular transversal section, a relatively large hyposome and a conspicuous bill-like projection. The longitudinal outline of T. robustum was oblong, widened in the middle, with an ellipsoidal transversal section, a small hyposome and a less prominent bill-like projection. Several morphological features of Katodinium glaucum (=Gyrodinium glaucum) resembled Gyrodinium, such as the cingular displacement, longitudinal ribs, trichocysts, rod-shaped and refractile bodies and a capsule that surrounded the spherical nucleus. Distinctive features of K. glaucum were the horseshoeshaped apical groove under a tongue-shaped notch pointed towards the dorsal side, and a bifurcated proximal end of the cingulum. Phylogenetic analysis revealed that Torodinium spp. and K. glaucum formed two independent lineages with no close relationships with other known dinoflagellates. The morphology of K. glaucum was distant from the type species of Katodinium. We propose the new genus and combination Lebouridinium glaucum gen. nov., comb. nov. for the species Katodinium glaucum.
RESUMO
The genus Balechina (=subgenus Pachydinium) was established for heterotrophic gymnodinioid dinoflagellates with a thick cell covering. The type species, B. pachydermata (=Gymnodinium pachyderm-atum), showed numerous fine longitudinal striae, whereas B. coerulea (=G. coeruleum) showed ~24 prominent longitudinal surface ridges or furrows and a distinctive blue pigmentation. We have investigated the morphology and molecular phylogeny of these taxa and the species Gymnodinium cucumis, G. lira and G. amphora from the western Mediterranean, Brazil and Japan. Sudden contractions at the cingulum level were seen in B. pachydermata, which also showed a high morphological variability which included morphotypes that have been described as Amphidinium vasculum, G. amphora, G. dogielii and G. gracile sensu Kofoid and Swezy. Molecular phylogeny based on small subunit rRNA gene sequences revealed that Balechina coerulea, G. cucumis and G. lira formed a clade distantly related to the clade of the type species, B. pachydermata, and G. amphora. We propose the new genus Cucumeridinium for the species with longitudinal ridges and a circular apical groove (Cucumeridinium coeruleum comb. nov., C. lira comb. nov. and C. cucumis comb. nov.), and Gymnodinium canus and G. costatum are considered synonyms of C. coeruleum. The genus Balechina remains for the species with a double-layer cell covering, bossed surface with fine striae, and an elongated elliptical apical groove. At present, the genus is monotypic containing only B. pachydermata.
RESUMO
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.
Assuntos
Carbonatos/metabolismo , Cianobactérias/metabolismo , Lagos/microbiologia , Biofilmes , Carbonatos/análise , Carbonatos/química , Cianobactérias/classificação , Cianobactérias/ultraestrutura , México , Microscopia Confocal , Filogenia , Pigmentos Biológicos/química , Análise Espectral RamanRESUMO
The Naica Mine in northern Mexico is famous for its giant gypsum crystals, which may reach up to 11 m long and contain fluid inclusions that might have captured microorganisms during their formation. These crystals formed under particularly stable geochemical conditions in cavities filled by low salinity hydrothermal water at 54-58°C. We have explored the microbial diversity associated to these deep, saline hydrothermal waters collected in the deepest (ca. 700-760 m) mineshafts by amplifying, cloning and sequencing small-subunit ribosomal RNA genes using primers specific for archaea, bacteria, and eukaryotes. Eukaryotes were not detectable in the samples and the prokaryotic diversity identified was very low. Two archaeal operational taxonomic units (OTUs) were detected in one sample. They clustered with, respectively, basal Thaumarchaeota lineages and with a large clade of environmental sequences branching at the base of the Thermoplasmatales within the Euryarchaeota. Bacterial sequences belonged to the Candidate Division OP3, Firmicutes and the Alpha- and Beta-proteobacteria. Most of the lineages detected appear autochthonous to the Naica system, since they had as closest representatives environmental sequences retrieved from deep sediments or the deep subsurface. In addition, the high GC content of 16S rRNA gene sequences belonging to the archaea and to some OP3 OTUs suggests that at least these lineages are thermophilic. Attempts to amplify diagnostic functional genes for methanogenesis (mcrA) and sulfate reduction (dsrAB) were unsuccessful, suggesting that those activities, if present, are not important in the aquifer. By contrast, genes encoding archaeal ammonium monooxygenase (AamoA) were amplified, suggesting that Naica Thaumarchaeota are involved in nitrification. These organisms are likely thermophilic chemolithoautotrophs adapted to thrive in an extremely energy-limited environment.
RESUMO
Cyanobacteria have affected major geochemical cycles (carbon, nitrogen, and oxygen) on Earth for billions of years. In particular, they have played a major role in the formation of calcium carbonates (i.e., calcification), which has been considered to be an extracellular process. We identified a cyanobacterium in modern microbialites in Lake Alchichica (Mexico) that forms intracellular amorphous calcium-magnesium-strontium-barium carbonate inclusions about 270 nanometers in average diameter, revealing an unexplored pathway for calcification. Phylogenetic analyses place this cyanobacterium within the deeply divergent order Gloeobacterales. The chemical composition and structure of the intracellular precipitates suggest some level of cellular control on the biomineralization process. This discovery expands the diversity of organisms capable of forming amorphous calcium carbonates.
Assuntos
Biofilmes , Carbonato de Cálcio/análise , Carbonatos/análise , Cianobactérias/isolamento & purificação , Cianobactérias/fisiologia , Corpos de Inclusão/química , Corpos de Inclusão/ultraestrutura , Lagos/microbiologia , Bário/análise , Sequência de Bases , Calcificação Fisiológica , Cálcio/análise , Carbonatos/metabolismo , Precipitação Química , Cianobactérias/classificação , Cianobactérias/ultraestrutura , Genes Bacterianos , Genes de RNAr , Magnésio/análise , México , Dados de Sequência Molecular , Filogenia , Estrôncio/análiseRESUMO
The geomicrobiology of crater lake microbialites remains largely unknown despite their evolutionary interest due to their resemblance to some Archaean analogs in the dominance of in situ carbonate precipitation over accretion. Here, we studied the diversity of archaea, bacteria and protists in microbialites of the alkaline Lake Alchichica from both field samples collected along a depth gradient (0-14 m depth) and long-term-maintained laboratory aquaria. Using small subunit (SSU) rRNA gene libraries and fingerprinting methods, we detected a wide diversity of bacteria and protists contrasting with a minor fraction of archaea. Oxygenic photosynthesizers were dominated by cyanobacteria, green algae and diatoms. Cyanobacterial diversity varied with depth, Oscillatoriales dominating shallow and intermediate microbialites and Pleurocapsales the deepest samples. The early-branching Gloeobacterales represented significant proportions in aquaria microbialites. Anoxygenic photosynthesizers were also diverse, comprising members of Alphaproteobacteria and Chloroflexi. Although photosynthetic microorganisms dominated in biomass, heterotrophic lineages were more diverse. We detected members of up to 21 bacterial phyla or candidate divisions, including lineages possibly involved in microbialite formation, such as sulfate-reducing Deltaproteobacteria but also Firmicutes and very diverse taxa likely able to degrade complex polymeric substances, such as Planctomycetales, Bacteroidetes and Verrucomicrobia. Heterotrophic eukaryotes were dominated by Fungi (including members of the basal Rozellida or Cryptomycota), Choanoflagellida, Nucleariida, Amoebozoa, Alveolata and Stramenopiles. The diversity and relative abundance of many eukaryotic lineages suggest an unforeseen role for protists in microbialite ecology. Many lineages from lake microbialites were successfully maintained in aquaria. Interestingly, the diversity detected in aquarium microbialites was higher than in field samples, possibly due to more stable and favorable laboratory conditions. The maintenance of highly diverse natural microbialites in laboratory aquaria holds promise to study the role of different metabolisms in the formation of these structures under controlled conditions.