Bacterial Dormancy Is More Prevalent in Freshwater than Hypersaline Lakes.
ABSTRACT: Bacteria employ a diverse array of strategies to survive under extreme environmental conditions but maintaining these adaptations comes at an energetic cost. If energy reserves drop too low, extremophiles may enter a dormant state to persist. We estimated bacterial dormancy and identified the environmental variables influencing our activity proxy in 10 hypersaline and freshwater lakes across the Western United States. Using ribosomal RNA:DNA ratios as an indicator for bacterial activity, we found that the proportion of the community exhibiting dormancy was 16% lower in hypersaline than freshwater lakes. Based on our indicator variable multiple regression results, saltier conditions in both freshwater and hypersaline lakes increased activity, suggesting that salinity was a robust environmental filter structuring bacterial activity in lake ecosystems. To a lesser degree, higher total phosphorus concentrations reduced dormancy in all lakes. Thus, even under extreme conditions, the competition for resources exerted pressure on activity. Within the compositionally distinct and less diverse hypersaline communities, abundant taxa were disproportionately active and localized in families Microbacteriaceae (Actinobacteria), Nitriliruptoraceae (Actinobacteria), and Rhodobacteraceae (Alphaproteobacteria). Our results are consistent with the view that hypersaline communities are able to capitalize on a seemingly more extreme, yet highly selective, set of conditions and finds that extremophiles may need dormancy less often to thrive and survive.
Project description:It is widely accepted that biodiversity is lower in more extreme environments. In this study, we sought to determine whether this trend, well documented for macroorganisms, also holds at the microbial level for bacteria. We used denaturing gradient gel electrophoresis (DGGE) with phylum-specific primers to quantify the taxon richness (i.e., the DGGE band numbers) of the bacterioplankton communities of 32 pristine Tibetan lakes that represent a broad salinity range (freshwater to hypersaline). For the lakes investigated, salinity was found to be the environmental variable with the strongest influence on the bacterial community composition. We found that the bacterial taxon richness in freshwater habitats increased with increasing salinity up to a value of 1‰. In saline systems (systems with >1‰ salinity), the expected decrease of taxon richness along a gradient of further increasing salinity was not observed. These patterns were consistently observed for two sets of samples taken in two different years. A comparison of 16S rRNA gene clone libraries revealed that the bacterial community of the lake with the highest salinity was characterized by a higher recent accelerated diversification than the community of a freshwater lake, whereas the phylogenetic diversity in the hypersaline lake was lower than that in the freshwater lake. These results suggest that different evolutionary forces may act on bacterial populations in freshwater and hypersaline lakes on the Tibetan Plateau, potentially resulting in different community structures and diversity patterns.
Project description:BACKGROUND:Hypersaline soda lakes are characterized by extreme high soluble carbonate alkalinity. Despite the high pH and salt content, highly diverse microbial communities are known to be present in soda lake brines but the microbiome of soda lake sediments received much less attention of microbiologists. Here, we performed metagenomic sequencing on soda lake sediments to give the first extensive overview of the taxonomic diversity found in these complex, extreme environments and to gain novel physiological insights into the most abundant, uncultured prokaryote lineages. RESULTS:We sequenced five metagenomes obtained from four surface sediments of Siberian soda lakes with a pH 10 and a salt content between 70 and 400 g L-1. The recovered 16S rRNA gene sequences were mostly from Bacteria, even in the salt-saturated lakes. Most OTUs were assigned to uncultured families. We reconstructed 871 metagenome-assembled genomes (MAGs) spanning more than 45 phyla and discovered the first extremophilic members of the Candidate Phyla Radiation (CPR). Five new species of CPR were among the most dominant community members. Novel dominant lineages were found within previously well-characterized functional groups involved in carbon, sulfur, and nitrogen cycling. Moreover, key enzymes of the Wood-Ljungdahl pathway were encoded within at least four bacterial phyla never previously associated with this ancient anaerobic pathway for carbon fixation and dissimilation, including the Actinobacteria. CONCLUSIONS:Our first sequencing effort of hypersaline soda lake sediment metagenomes led to two important advances. First, we showed the existence and obtained the first genomes of haloalkaliphilic members of the CPR and several hundred other novel prokaryote lineages. The soda lake CPR is a functionally diverse group, but the most abundant organisms in this study are likely fermenters with a possible role in primary carbon degradation. Second, we found evidence for the presence of the Wood-Ljungdahl pathway in many more taxonomic groups than those encompassing known homo-acetogens, sulfate-reducers, and methanogens. Since only few environmental metagenomics studies have targeted sediment microbial communities and never to this extent, we expect that our findings are relevant not only for the understanding of haloalkaline environments but can also be used to set targets for future studies on marine and freshwater sediments.
Project description:The influence of altitude and salinity on bacterioplankton community composition (BCC) in 16 high-mountain lakes located at altitudes of 2,817 to 5,134 m on the Eastern Qinghai-Xizang (Tibetan) Plateau, China, spanning a salinity gradient from 0.02% (freshwater) to 22.3% (hypersaline), was investigated. Three different methods, fluorescent in situ hybridization, denaturing gradient gel electrophoresis (DGGE) with subsequent band sequencing, and reverse line blot hybridization (RLB) with probes targeting 17 freshwater bacterial groups, were used for analysis of BCC. Furthermore, the salt tolerances of 47 strains affiliated with groups detected in or isolated from the Tibetan habitats were investigated. Altitude was not found to influence BCC significantly within the investigated range. Several groups of typical freshwater bacteria, e.g., the ACK-M1 cluster and the Polynucleobacter group, were detected in habitats located above 4,400 m. Salinity was found to be the dominating environmental factor controlling BCC in the investigated lakes, resulting in only small overlaps in the BCCs of freshwater and hypersaline lakes. The relative abundances of different classes of Proteobacteria showed a sharp succession along the salinity gradient. Both DGGE and RLB demonstrated that a few freshwater bacterial groups, e.g., GKS98 and LD2, appeared over wide salinity ranges. Six freshwater isolates affiliated with the GKS98 cluster grew in ecophysiological experiments at maximum salinities of 0.3% to 0.7% (oligosaline), while this group was detected in habitats with salinities up to 6.7% (hypersaline). This observation indicated ecologically significant differences in ecophysiological adaptations among members of this narrow phylogenetic group and suggested ecological significance of microdiversity.
Project description:All known ammonia-oxidizing archaea (AOA) belong to the phylum Thaumarchaeota within the domain Archaea. AOA possess the diagnostic amoA gene (encoding the alpha subunit of ammonia monooxygenase) and produce lipid biomarker thaumarchaeol. Although the abundance and diversity of amoA gene-encoding archaea (AEA) in freshwater lakes have been well-studied, little is known about AEA ecology in saline/hypersaline lakes. In this study, the distribution of the archaeal amoA gene and thaumarchaeol were investigated in nine Qinghai-Tibetan lakes with a salinity range from freshwater to salt-saturation (salinity: 325 g L(-) (1)). The results showed that the archaeal amoA gene was present in hypersaline lakes with salinity up to 160 g L(-) (1). The archaeal amoA gene diversity in Tibetan lakes was different from those in other lakes worldwide, suggesting Tibetan lakes (high elevation, strong ultraviolet, and dry climate) may host a unique AEA population of different evolutionary origin from those in other lakes. Thaumarchaeol was present in all of the studied hypersaline lakes, even in those where no AEA amoA gene was observed. Future research is needed to determine the ecological function of AEA and possible sources of thaumarchaeol in the Qinghai-Tibetan hypersaline lakes.
Project description:Subglacial lakes are unique environments that, despite the extreme dark and cold conditions, have been shown to host microbial life. Many subglacial lakes have been discovered beneath the ice sheets of Antarctica and Greenland, but no spatially isolated water body has been documented as hypersaline. We use radio-echo sounding measurements to identify two subglacial lakes situated in bedrock troughs near the ice divide of Devon Ice Cap, Canadian Arctic. Modeled basal ice temperatures in the lake area are no higher than -10.5°C, suggesting that these lakes consist of hypersaline water. This implication of hypersalinity is in agreement with the surrounding geology, which indicates that the subglacial lakes are situated within an evaporite-rich sediment unit containing a bedded salt sequence, which likely act as the solute source for the brine. Our results reveal the first evidence for subglacial lakes in the Canadian Arctic and the first hypersaline subglacial lakes reported to date. We conclude that these previously unknown hypersaline subglacial lakes may represent significant and largely isolated microbial habitats, and are compelling analogs for potential ice-covered brine lakes and lenses on planetary bodies across the solar system.
Project description:Bacteria play a key role in freshwater biogeochemical cycling, but long-term trends in freshwater bacterial community composition and dynamics are not yet well characterized. We used a multiyear time series of 16S rRNA gene amplicon sequencing data from eight bog lakes to census the freshwater bacterial community and observe annual and seasonal trends in abundance. The sites that we studied encompassed a range of water column mixing frequencies, which we hypothesized would be associated with trends in alpha and beta diversity. Each lake and layer contained a distinct bacterial community, with distinct levels of richness and indicator taxa that likely reflected the environmental conditions of each lake type sampled, including Actinobacteria in polymictic lakes (i.e., lakes with multiple mixing events per year), Methylophilales in dimictic lakes (lakes with two mixing events per year, usually in spring and fall), and "Candidatus Omnitrophica" in meromictic lakes (lakes with no recorded mixing events). The community present during each year at each site was also surprisingly unique. Despite unexpected interannual variability in community composition, we detected a core community of taxa found in all lakes and layers, including Actinobacteria tribe acI-B2 and Betaprotobacteria lineage PnecC. Although trends in abundance did not repeat annually, each freshwater lineage within the communities had a consistent lifestyle, defined by persistence, abundance, and variability. The results of our analysis emphasize the importance of long-term multisite observations, as analyzing only a single year of data or one lake would not have allowed us to describe the dynamics and composition of these freshwater bacterial communities to the extent presented here. IMPORTANCE Lakes are excellent systems for investigating bacterial community dynamics because they have clear boundaries and strong environmental gradients. The results of our research demonstrate that bacterial community composition varies by year, a finding which likely applies to other ecosystems and has implications for study design and interpretation. Understanding the drivers and controls of bacterial communities on long time scales would improve both our knowledge of fundamental properties of bacterial communities and our ability to predict community states. In this specific ecosystem, bog lakes play a disproportionately large role in global carbon cycling, and the information presented here may ultimately help refine carbon budgets for these lakes. Finally, all data and code in this study are publicly available. We hope that this will serve as a resource for anyone seeking to answer their own microbial ecology questions using a multiyear time series.
Project description:Saline lakes are intriguing ecosystems harboring extremely productive microbial communities in spite of their extreme environmental conditions. We performed a comprehensive analysis of the genetic diversity (18S rRNA gene) of the planktonic microbial eukaryotes (nano- and picoeukaryotes) in six different inland saline lakes located in the Qaidam Basin. The novelty level are high, with about 11.23% of the whole dataset showing <90% identity to any previously reported sequence in GenBank. At least 4 operational taxonomic units (OTUs) in mesosaline lakes, while up to eighteen OTUs in hypersaline lakes show very low CCM and CEM scores, indicating that these sequences are highly distantly related to any existing sequence. Most of the 18S rRNA gene sequence reads obtained in investigated mesosaline lakes is closely related to Holozoa group (48.13%), whereas Stramenopiles (26.65%) and Alveolates (10.84%) are the next most common groups. Hypersaline lakes in the Qaidam Basin are also dominated by Holozoa group, accounting for 26.65% of the total number of sequence reads. Notably, Chlorophyta group are only found in high abundance in Lake Gasikule (28.00%), whereas less represented in other hypersaline lakes such as Gahai (0.50%) and Xiaochaidan (1.15%). Further analysis show that the compositions of planktonic eukaryotic assemblages are also most variable between different sampling sites in the same lake. Out of the parameters, four show significant correlation to this CCA: altitude, calcium, sodium and potassium concentrations. Overall, this study shows important gaps in the current knowledge about planktonic microbial eukaryotes inhabiting Qaidam Basin (hyper) saline water bodies. The identified diversity and novelty patterns among eukaryotic plankton assemblages in saline lake are of great importance for understanding and interpreting their ecology and evolution.
Project description:In this work, molecular diversity of two hypersaline microbial mats was compared by Whole Genome Shotgun (WGS) sequencing of environmental DNA from the mats. Brava and Tebenquiche are lakes in the Salar de Atacama, Chile, where microbial communities are growing in extreme conditions, including high salinity, high solar irradiance, and high levels of toxic metals and metaloids. Evaporation creates hypersaline conditions in these lakes and mineral precipitation is a characteristic geomicrobiological feature of these benthic ecosystems. The mat from Brava was more rich and diverse, with a higher number of different taxa and with species more evenly distributed. At the phylum level, Proteobacteria, Cyanobacteria, Chloroflexi, Bacteroidetes and Firmicutes were the most abundant, including ~75% of total sequences. At the genus level, the most abundant sequences were affilitated to anoxygenic phototropic and cyanobacterial genera. In Tebenquiche mats, Proteobacteria and Bacteroidetes covered ~70% of the sequences, and 13% of the sequences were affiliated to Salinibacter genus, thus addressing the lower diversity. Regardless of the differences at the taxonomic level, functionally the two mats were similar. Thus, similar roles could be fulfilled by different organisms. Carbon fixation through the Wood-Ljungdahl pathway was well represented in these datasets, and also in other mats from Andean lakes. In spite of presenting less taxonomic diversity, Tebenquiche mats showed increased abundance and variety of rhodopsin genes. Comparison with other metagenomes allowed identifying xantorhodopsins as hallmark genes not only from Brava and Tebenquiche mats, but also for other mats developing at high altitudes in similar environmental conditions.
Project description:Organisms that can grow in extreme conditions would be expected to be confined to extreme environments. However, we were able to capture highly productive communities of algae and bacteria capable of growing in acidic (pH 2), basic (pH 12) and saline (40 ppt) conditions from an ordinary freshwater lake. Microbial communities may thus include taxa that are highly productive in conditions that are far outside the range of conditions experienced in their host ecosystem. The organisms we captured were not obligate extremophiles, but were capable of growing in both extreme and benign conditions. The ability to grow in extreme conditions may thus be a common functional attribute in microbial communities.
Project description:In order to investigate the factors controlling the bacterial community composition (BCC) in reservoirs, we sampled three freshwater reservoirs with contrasted physical and chemical characteristics and trophic status. The BCC was analysed by 16S rRNA gene amplicon 454 pyrosequencing. In parallel, a complete dataset of environmental parameters and phytoplankton community composition was also collected. BCC in the analysed reservoirs resembled that of epilimnetic waters of natural freshwater lakes with presence of Actinobacteria, Alpha- and Betaproteobacteria, Cytophaga-Flavobacteria-Bacteroidetes (CFB) and Verrucomicrobia groups. Our results evidenced that the retrieved BCC in the analysed reservoirs was strongly influenced by pH, alkalinity and organic carbon content, whereas comparatively little change was observed among layers in stratified conditions.