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Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake

ABSTRACT: Cueva de la Mora is a permanently stratified acidic pit lake with extremely high concentrations of heavy metals at depth. In order to evaluate the potential for in situ sulfide production, we characterized the microbial community in the deep layer using metagenomics and metatranscriptomics. We retrieved 18 high quality metagenome-assembled genomes (MAGs) representing the most abundant populations. None of the MAGs were closely related to either cultured or non-cultured organisms from the Genome Taxonomy or NCBI databases (none with average nucleotide identity >95%). Despite oxygen concentrations that are consistently below detection in the deep layer, some archaeal and bacterial MAGs mapped transcripts of genes for sulfide oxidation coupled with oxygen reduction. Among these microaerophilic sulfide oxidizers, mixotrophic Thermoplasmatales archaea were the most numerous and represented 24% of the total community. Populations associated with the highest predicted in situ activity for sulfate reduction were affiliated with Actinobacteria, Chloroflexi, and Nitrospirae phyla, and together represented about 9% of the total community. These MAGs, in addition to a less abundant Proteobacteria MAG in the genus Desulfomonile, contained transcripts of genes in the Wood-Ljungdahl pathway. All MAGs had significant genetic potential for organic carbon oxidation. Our results indicate that novel acidophiles are contributing to biosulfidogenesis in the deep layer of Cueva de la Mora, and that in situ sulfide production is limited by organic carbon availability and sulfur oxidation.

SUBMITTER: Ayala-Munoz D

PROVIDER: S-EPMC9326234 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Cueva de la Mora (CM) is an acidic, meromictic pit lake in the Iberian Pyrite Belt characterized by extremely high metal(loid) concentrations and strong gradients in oxygen, metal, and nutrient concentrations. We hypothesized that geochemical variations with depth would result in differences in community composition and in metal resistance strategies among active microbial populations. We also hypothesized that metal resistance gene (MRG) expression would correlate with toxicity levels for dissolved metal species in the lake. Water samples were collected in the upper oxic layer, chemocline, and deep anoxic layer of the lake for shotgun metagenomic and metatranscriptomic sequencing. Metagenomic analyses revealed dramatic differences in the composition of the microbial communities with depth, consistent with changing geochemistry. Based on relative abundance of taxa identified in each metagenome, Eukaryotes (predominantly Coccomyxa) dominated the upper layer, while Archaea (predominantly Thermoplasmatales) dominated the deep layer, and a combination of Bacteria and Eukaryotes were abundant at the chemocline. We compared metal resistance across communities using a curated list of protein-coding MRGs with KEGG Orthology identifiers (KOs) and found that there were broad differences in the metal resistance strategies (e.g., intracellular metal accumulation) expressed by Eukaryotes, Bacteria, and Archaea. Although normalized abundances of MRG and MRG expression were generally higher in the deep layer, expression of metal-specific genes was not strongly related to variations in specific metal concentrations, especially for Cu and As. We also compared MRG potential and expression in metagenome assembled genomes (MAGs) from the deep layer, where metal concentrations are highest. Consistent with previous work showing differences in metal resistance mechanisms even at the strain level, MRG expression patterns varied strongly among MAG populations from the same depth. Some MAG populations expressed very few MRG known to date, suggesting that novel metal resistance strategies remain to be discovered in uncultivated acidophiles.

Project description:Subglacial microbial habitats are widespread in glaciated regions of our planet. Some of these environments have been isolated from the atmosphere and from sunlight for many thousands of years. Consequently, ecosystem processes must rely on energy gained from the oxidation of inorganic substrates or detrital organic matter. Subglacial Lake Whillans (SLW) is one of more than 400 subglacial lakes known to exist under the Antarctic ice sheet; however, little is known about microbial physiology and energetics in these systems. When it was sampled through its 800 m thick ice cover in 2013, the SLW water column was shallow (~2 m deep), oxygenated, and possessed sufficient concentrations of C, N, and P substrates to support microbial growth. Here, we use a combination of physiological assays and models to assess the energetics of microbial life in SLW. In general, SLW microorganisms grew slowly in this energy-limited environment. Heterotrophic cellular carbon turnover times, calculated from 3H-thymidine and 3H-leucine incorporation rates, were long (60 to 500 days) while cellular doubling times averaged 196 days. Inferred growth rates (average ~0.006 d-1) obtained from the same incubations were at least an order of magnitude lower than those measured in Antarctic surface lakes and oligotrophic areas of the ocean. Low growth efficiency (8%) indicated that heterotrophic populations in SLW partition a majority of their carbon demand to cellular maintenance rather than growth. Chemoautotrophic CO2-fixation exceeded heterotrophic organic C-demand by a factor of ~1.5. Aerobic respiratory activity associated with heterotrophic and chemoautotrophic metabolism surpassed the estimated supply of oxygen to SLW, implying that microbial activity could deplete the oxygenated waters, resulting in anoxia. We used thermodynamic calculations to examine the biogeochemical and energetic consequences of environmentally imposed switching between aerobic and anaerobic metabolisms in the SLW water column. Heterotrophic metabolisms utilizing acetate and formate as electron donors yielded less energy than chemolithotrophic metabolisms when calculated in terms of energy density, which supports experimental results that showed chemoautotrophic activity in excess of heterotrophic activity. The microbial communities of subglacial lake ecosystems provide important natural laboratories to study the physiological and biogeochemical behavior of microorganisms inhabiting cold, dark environments.

Project description:Base Mine Lake (BML) is the first full-scale demonstration end pit lake for the oil sands mining industry in Canada. We examined aerobic methanotrophic bacteria over all seasons for 5 years in this dimictic lake. Methanotrophs comprised up to 58% of all bacterial reads in 16S rRNA gene amplicon sequencing analyses (median 2.8%), and up to 2.7 × 104 cells mL-1 of water (median 0.5 × 103) based on qPCR of pmoA genes. Methanotrophic activity and populations in the lake water were highest during fall turnover and remained high through the winter ice-covered period into spring turnover. They declined during summer stratification, especially in the epilimnion. Three methanotroph genera (Methylobacter, Methylovulum, and Methyloparacoccus) cycled seasonally, based on both relative and absolute abundance measurements. Methylobacter and Methylovulum populations peaked in winter/spring, when methane oxidation activity was psychrophilic. Methyloparacoccus populations increased in the water column through summer and fall, when methane oxidation was mesophilic, and also predominated in the underlying tailings sediment. Other, less abundant genera grew primarily during summer, possibly due to distinct CH4/O2 microniches created during thermal stratification. These data are consistent with temporal and spatial niche differentiation based on temperature, CH4 and O2. This pit lake displays methane cycling and methanotroph population dynamics similar to natural boreal lakes. IMPORTANCE The study examined methanotrophic bacteria in an industrial end pit lake, combining molecular DNA methods (both quantitative and descriptive) with biogeochemical measurements. The lake was sampled over 5 years, in all four seasons, as often as weekly, and included sub-ice samples. The resulting multiseason and multiyear data set is unique in its size and intensity, and allowed us to document clear and consistent seasonal patterns of growth and decline of three methanotroph genera (Methylobacter, Methylovulum, and Methyloparacoccus). Laboratory experiments suggested that one major control of this succession was niche partitioning based on temperature. The study helps to understand microbial dynamics in engineered end pit lakes, but we propose that the dynamics are typical of boreal stratified lakes and widely applicable in microbial ecology and limnology. Methane-oxidizing bacteria are important model organisms in microbial ecology and have implications for global climate change.

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Novel Microorganisms Contribute to Biosulfidogenesis in the Deep Layer of an Acidic Pit Lake

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