In situ phosphatization and reductive cell division have recently been discovered within the vacuolate sulphur-oxidizing bacteria. Here we show that certain Neoproterozoic Doushantuo Formation (about 600 million years bp) microfossils, including structures previously interpreted as the oldest known metazoan eggs and embryos, can be interpreted as giant vacuolate sulphur bacteria. Sulphur bacteria of the genus Thiomargarita have sizes and morphologies similar to those of many Doushantuo microfossils, including symmetrical cell clusters that result from multiple stages of reductive division in three planes. We also propose that Doushantuo phosphorite precipitation was mediated by these bacteria, as shown in modern Thiomargarita-associated phosphogenic sites, thus providing the taphonomic conditions that preserved other fossils known from the Doushantuo Formation.
Methylmercury (MeHg) is a bioaccumulative neurotoxin that is produced by certain anaerobic microorganisms, but the abundance and importance of different methylating populations in the environment is not well understood. We combined mercury geochemistry, hgcA gene cloning, rRNA methods, and metagenomics to compare microbial communities associated with MeHg production in two sulfate-impacted lakes on Minnesota's Mesabi Iron Range. The two lakes represent regional endmembers among sulfate-impacted sites in terms of their dissolved sulfide concentrations and MeHg production potential. rRNA amplicon sequencing indicates that sediments and anoxic bottom waters from both lakes contained diverse communities with multiple clades of sulfate reducing Deltaproteobacteria and Clostridia. In hgcA gene clone libraries, however, hgcA sequences were from taxa associated with methanogenesis and iron reduction in addition to sulfate reduction, and the most abundant clones were from unknown groups. We therefore applied metagenomics to identify the unknown populations in the lakes with the capability to methylate mercury, and reconstructed 27 genomic bins with hgcA. Some of the most abundant potential methylating populations were from phyla that are not typically associated with MeHg production, including a relative of the Aminicenantes (formerly candidate phylum OP8) and members of the Kiritimatiellaeota (PVC superphylum) and Spirochaetes that, together, were more than 50% of the potential methylators in some samples. These populations do not have genes for sulfate reduction, and likely degrade organic compounds by fermentation or other anaerobic processes. Our results indicate that previously unrecognized populations with hgcAB are abundant and may be important for MeHg production in some freshwater ecosystems.
Large, colorless sulfur-oxidizing bacteria (LSB) of the family Beggiatoaceae form thick mats at sulfidic sediment surfaces, where they efficiently detoxify sulfide before it enters the water column. The genus Thiomargarita harbors the largest known free-living bacteria with cell sizes of up to 750 μm in diameter. In addition to their ability to oxidize reduced sulfur compounds, some Thiomargarita spp. are known to store large amounts of nitrate, phosphate and elemental sulfur internally. To date little is known about their energy yielding metabolic pathways, and how these pathways compare to other Beggiatoaceae. Here, we present a draft single-cell genome of a chain-forming “Candidatus Thiomargarita nelsonii Thio36”, and conduct a comparative analysis to five draft and one full genome of other members of the Beggiatoaceae. “Ca. T. nelsonii Thio36” is able to respire nitrate to both ammonium and dinitrogen, which allows them to flexibly respond to environmental changes. Genes for sulfur oxidation and inorganic carbon fixation confirmed that “Ca. T. nelsonii Thio36” can function as a chemolithoautotroph. Carbon can be fixed via the Calvin–Benson–Bassham cycle, which is common among the Beggiatoaceae. In addition we found key genes of the reductive tricarboxylic acid cycle that point toward an alternative CO2 fixation pathway. Surprisingly, “Ca. T. nelsonii Thio36” also encodes key genes of the C2-cycle that convert 2-phosphoglycolate to 3-phosphoglycerate during photorespiration in higher plants and cyanobacteria. Moreover, we identified a novel trait of a flavin-based energy bifurcation pathway coupled to a Na+-translocating membrane complex (Rnf). The coupling of these pathways may be key to surviving long periods of anoxia. As other Beggiatoaceae “Ca. T. nelsonii Thio36” encodes many genes similar to those of (filamentous) cyanobacteria. In summary, the genome of “Ca. T. nelsonii Thio36” provides additional insight into the ecology of giant sulfur-oxidizing bacteria, and reveals unique genomic features for the Thiomargarita lineage within the Beggiatoaceae.
The large sulphur bacteria, first discovered in the early nineteenth century, include some of the largest bacteria identified to date. Individual cells are often visible to the unaided eye and can reach 750 μm in diameter. The cells usually feature light-refracting inclusions of elemental sulphur and a large internal aqueous vacuole, which restricts the cytoplasm to the outermost periphery. In some taxa, it has been demonstrated that the vacuole can also serve for the storage of high millimolar concentrations of nitrate. Over the course of the past two centuries, a wide range of morphological variation within the family Beggiatoaceae has been found. However, representatives of this clade are frequently recalcitrant to current standard microbiological techniques, including 16S rRNA gene sequencing and culturing, and a reliable classification of these bacteria is often complicated. Here we present a summary of the efforts made and achievements accomplished in the past years, and give perspectives for investigating the heterogeneity and possible evolutionary developments in this extraordinary group of bacteria.
The genus Thiomargarita includes the world's largest bacteria. But as uncultured organisms, their physiology, metabolism, and basis for their gigantism are not well understood. Thus, a genomics approach, applied to a single Candidatus Thiomargarita nelsonii cell was employed to explore the genetic potential of one of these enigmatic giant bacteria. The Thiomargarita cell was obtained from an assemblage of budding Ca. T. nelsonii attached to a provannid gastropod shell from Hydrate Ridge, a methane seep offshore of Oregon, USA. Here we present a manually curated genome of Bud S10 resulting from a hybrid assembly of long Pacific Biosciences and short Illumina sequencing reads. With respect to inorganic carbon fixation and sulfur oxidation pathways, the Ca. T. nelsonii Hydrate Ridge Bud S10 genome was similar to marine sister taxa within the family Beggiatoaceae. However, the Bud S10 genome contains genes suggestive of the genetic potential for lithotrophic growth on arsenite and perhaps hydrogen. The genome also revealed that Bud S10 likely respires nitrate via two pathways: a complete denitrification pathway and a dissimilatory nitrate reduction to ammonia pathway. Both pathways have been predicted, but not previously fully elucidated, in the genomes of other large, vacuolated, sulfur-oxidizing bacteria. Surprisingly, the genome also had a high number of unusual features for a bacterium to include the largest number of metacaspases and introns ever reported in a bacterium. Also present, are a large number of other mobile genetic elements, such as insertion sequence (IS) transposable elements and miniature inverted-repeat transposable elements (MITEs). In some cases, mobile genetic elements disrupted key genes in metabolic pathways. For example, a MITE interrupts hupL, which encodes the large subunit of the hydrogenase in hydrogen oxidation. Moreover, we detected a group I intron in one of the most critical genes in the sulfur oxidation pathway, dsrA. The dsrA group I intron also carried a MITE sequence that, like the hupL MITE family, occurs broadly across the genome. The presence of a high degree of mobile elements in genes central to Thiomargarita's core metabolism has not been previously reported in free-living bacteria and suggests a highly mutable genome.
The formation of marine phosphatic mineral deposits remains incompletely understood, despite decades of research. The involvement of bacteria in this process has long been suspected, and both modern and ancient associations between bacteria and phosphorites have been recorded. Only recently has a specific bacterial metabolic process associated with the formation of phosphorites been discovered. Recent studies demonstrate that polyphosphate utilization by sulfide-oxidizing bacteria results in the rapid precipitation of apatite – providing at least a partial mechanism to explain the close spatial correlation between accumulations of sulfide-oxidizing bacteria and modern phosphorites. Possible fossilized bacteria are known from ancient phosphatic mineral deposits. Potentially, the fossilized cells represent the remains of bacteria that induced the formation of those phosphorites. However, robust criteria for the recognition of these bacteria have yet to be identified.
Marine phosphate-rich sedimentary deposits (phosphorites) are important geological reservoirs for the biologically essential nutrient phosphorous. Phosphorites first appear in abundance approximately 600 million years ago, but their proliferation at that time is poorly understood. Recent marine phosphorites spatially correlate with the habitats of vacuolated sulfide-oxidizing bacteria that store polyphosphates under oxic conditions to be utilized under sulfidic conditions. Hydrolysis of the stored polyphosphate results in the rapid precipitation of the phosphate-rich mineral apatite-providing a mechanism to explain the association between modern phosphorites and these bacteria. Whether sulfur bacteria were important to the formation of ancient phosphorites has been unresolved. Here, we present the remains of modern sulfide-oxidizing bacteria that are partially encrusted in apatite, providing evidence that bacterially mediated phosphogenesis can rapidly permineralize sulfide-oxidizing bacteria and perhaps other types of organic remains. We also describe filamentous microfossils that resemble modern sulfide-oxidizing bacteria from two major phosphogenic episodes in the geologic record. These microfossils contain sulfur-rich inclusions that may represent relict sulfur globules, a diagnostic feature of modern sulfide-oxidizing bacteria. These findings suggest that sulfur bacteria, which are known to mediate the precipitation of apatite in modern sediments, were also present in certain phosphogenic settings for at least the last 600 million years. If polyphosphate-utilizing sulfide-oxidizing bacteria also played a role in the formation of ancient phosphorites, their requirements for oxygen, or oxygen-requiring metabolites such as nitrate, might explain the temporal correlation between the first appearance of globally distributed marine phosphorites and increasing oxygenation of Neoproterozoic oceans.
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