Biology subjects

Pester, M.

Publications and source records attributed to Pester, M..

4 recordsLinked to original sources

bioRxiv2018

Pyrite formation from FeS and H2S is mediated by a novel type of microbial energy metabolism

The exergonic reaction of FeS with H2S to form FeS2 (pyrite) and H2 was postulated to have operated as an early form of energy metabolism on primordial Earth. Since the Archean, sedimentary pyrite formation played a major role in the global iron and sulfur cycles, with direct impact on the redox chemistry of the atmosphere. To date, pyrite formation was considered a purely geochemical reaction. Here, we present microbial enrichment cultures, which grew with FeS, H2S, and CO2 as their sole substrates to produce FeS2 and CH4. Cultures grew over periods of three to eight months to cell densities of up to 2-9x106 cells mL-1. Transformation of FeS with H2S to FeS2 was followed by 57Fe Mossbauer spectroscopy and showed a clear biological temperature profile with maximum activity at 28{degrees}C and decreasing activities towards 4{degrees}C and 60{degrees}C. CH4 was formed concomitantly with FeS2 and exhibited the same temperature dependence. Addition of either penicillin or 2-bromoethanesulfonate inhibited both FeS2 and CH4 production, indicating a syntrophic coupling of pyrite formation to methanogenesis. This hypothesis was supported by a 16S rRNA gene-based phylogenetic analysis, which identified at least one archaeal and five bacterial species. The archaeon was closely related to the hydrogenotrophic methanogen Methanospirillum stamsii while the bacteria were most closely related to sulfate-reducing Deltaproteobacteria, as well as uncultured Firmicutes and Actinobacteria. We identified a novel type of microbial metabolism able to conserve energy from FeS transformation to FeS2, which may serve as a model for a postulated primordial iron-sulfur world.\n\nSignificance statementPyrite is the most abundant iron-sulfur mineral in sediments. Over geological times, its burial controlled oxygen levels in the atmosphere and sulfate concentrations in seawater. Its formation in sediments is so far considered a purely geochemical process that is at most indirectly supported by microbial activity. We show that lithotrophic microorganisms can directly transform FeS and H2S to FeS2 and use this exergonic reaction as a novel form of energy metabolism that is syntrophically coupled to methanogenesis. Our results provide insights into a syntrophic relationship that could sustain part of the deep biosphere and lend support to the iron-sulfur-world theory that postulated FeS transformation to FeS2 as a key energy-delivering reaction for life to emerge.

microbiology↗

bioRxiv2018

Growth arrest in the active rare biosphere

Microbial diversity in the environment is mainly concealed within the rare biosphere, which is arbitrarily defined as all species with <0.1% relative abundance. While dormancy explains a low-abundance state very well, the cellular mechanisms leading to rare but active microorganisms are not clear. We used environmental systems biology to genomically and metabolically characterize a cosmopolitan sulfate reducer that is of low abundance but highly active in peat soil, where it contributes to counterbalance methane emissions. We obtained a 98%-complete genome of this low-abundance species, Candidatus Desulfosporosinus infrequens, by metagenomics. To test for environmentally relevant metabolic activity of Ca. D. infrequens, anoxic peat soil microcosms were incubated under diverse in situ-like conditions for 36 days and analyzed by metatranscriptomics. Compared to the no-substrate control, transcriptional activity of Ca. D. infrequens increased 56- to 188-fold in incubations with sulfate and acetate, propionate, lactate, or butyrate, revealing a versatile substrate use. Cellular activation was due to a significant overexpression of genes encoding ribosomal proteins, dissimilatory sulfate reduction, and carbon-degradation pathways, but not of genes encoding DNA or cell replication. We show for the first time that a rare biosphere member transcribes metabolic pathways relevant for carbon and sulfur cycling over prolonged time periods while being growth-arrested in its lag phase.\n\nSignificanceThe microbial rare biosphere represents the largest pool of biodiversity on Earth and constitutes, in sum of all its members, a considerable part of a habitats biomass. Dormancy or starvation are typically used to explain a low-abundance state. We show that low-abundance microorganisms can be highly metabolically active while being growth-arrested over prolonged time periods. We show that this is true for microbial keystone species, such as a cosmopolitan but low-abundance sulfate reducer in wetlands that is involved in counterbalancing greenhouse gas emission. Our results challenge the central dogmas \"metabolic activity translates directly into growth\" as well as \"low abundance equals little ecosystem impact\" and provide an important step forward in understanding rare biosphere members relevant for ecosystem functions.

microbiology↗

bioRxiv2017

Peatland Acidobacteria with a dissimilatory sulfur metabolism

Sulfur-cycling microorganisms impact organic matter decomposition in wetlands and consequently greenhouse gas emissions from these globally relevant environments. However,their identities and physiological properties are largely unknown. By applying a functional metagenomics approach to an acidic peatland, we recovered draft genomes of seven novel Acidobacteria species with the potential for dissimilatory sulfite (dsrAB, dsrC, dsrD, dsrN, dsrT, dsrMKJOP) or sulfate respiration (sat, aprBA, qmoABC plus dsr genes). Surprisingly, the genomes also encoded dsrL, a unique gene of the sulfur oxidation pathway. Metatranscriptome analysis demonstrated expression of acidobacterial sulfur-metabolism genes in native peat soil and their upregulation in diverse anoxic microcosms. This indicated an active sulfate respiration pathway, which, however, could also operate in reverse for sulfur oxidation as recently shown for other microorganisms. Acidobacteria that only harbored genes for sulfite reduction additionally encoded enzymes that liberate sulfite from organosulfonates, which suggested organic sulfur compounds as complementary energy sources. Further metabolic potentials included polysaccharide hydrolysis and sugar utilization, aerobic respiration, several fermentative capabilities, and hydrogen oxidation. Our findings extend both, the known physiological and genetic properties of Acidobacteria and the known taxonomic diversity of microorganisms with a DsrAB-based sulfur metabolism, and highlight new fundamental niches for facultative anaerobic Acidobacteria in wetlands based on exploitation of inorganic and organic sulfur molecules for energy conservation.

microbiology↗

bioRxiv2017

Rice paddy Nitrospirae encode and express genes related to sulfate respiration: proposal of the new genus Candidatus Sulfobium

Nitrospirae spp. distantly related to thermophilic, sulfate-reducing Thermodesulfovibrio species are regularly observed in environmental surveys of anoxic marine and freshwater habitats. However, little is known about their genetic make-up and physiology. Here, we present the draft genome of Nitrospirae bacterium Nbg-4 as a representative of this clade and analyzed its in situ protein expression under sulfate-enriched and sulfate-depleted conditions in rice paddy soil. The genome of Nbg-4 was assembled from replicated metagenomes of rice paddy soil that was used to grow rice plants in the presence and absence of gypsum (CaSO4x2H2O). Nbg-4 encoded the full pathway of dissimilatory sulfate reduction and showed expression thereof in gypsum-amended anoxic bulk soil as revealed by parallel metaproteomics. In addition, Nbg-4 encoded the full pathway of dissimilatory nitrate reduction to ammonia, which was expressed in bulk soil without gypsum amendment. The relative abundance of Nbg-4-related metagenome reads was similar under both treatments indicating that it maintained stable populations while shifting its energy metabolism. Further genome reconstruction revealed the potential to utilize butyrate, formate, H2, or acetate as electron donor, with the Wood-Ljungdahl pathway being expressed under both conditions. Comparison to publicly available Nitrospirae genome bins confirmed that the pathway for dissimilatory sulfate reduction is also present in related Nitrospirae recovered from groundwater. Subsequent phylogenomics showed that such microorganisms form a novel genus within the phylum Nitrospirae, with Nbg-4 as a representative species. Based on the widespread occurrence of this novel genus, we propose for Nbg-4 the name Candidatus Sulfobium mesophilum, gen. nov., spec. nov.\n\nImportanceRice paddies are indispensable for food supply but are a major source of the greenhouse gas methane. If not counterbalanced by cryptic sulfur cycling, methane emission from rice paddy fields would be even higher. However, the microorganisms involved in this sulfur cycling are little understood. By using an environmental systems biology approach of Italian rice paddy soil, we could retrieve the population genome of a novel member of the phylum Nitrospirae. This microorganism encoded the full pathway of dissimilatory sulfate reduction and expressed it in situ under sulfate-enriched and anoxic conditions. Phylogenomics and comparison to environmental surveys showed that such microorganisms are actually widespread in freshwater and marine environments. At the same time, they represent a yet undiscovered genus within the little explored Nitrospirae. Our results will be important to design enrichment strategies and postgenomic studies to fully understand the contribution of these novel Nitrospirae to the global sulfur cycle.

microbiology↗