Comprehensive Insights Into Composition, Metabolic Potentials, and Interactions Among Archaeal, Bacterial, and Viral Assemblages in Meromictic Lake Shunet in Siberia

Wu, Yuting; Yang, Cheng‐Yu; Chiang, Pei‐Wen; Tseng, Chwan-Lu; Chiu, Hsiu‐Hui; Saeed, Isaam; Baatar, Bayanmunkh; Rogozin, D. Yu.; Halgamuge, Saman K.; Дегерменджи, А. Г.; Tang, Sen‐Lin

doi:10.3389/fmicb.2018.01763

Cited by 11 publications

(23 citation statements)

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“…A study from Lake Biwa (38) reported that Ͼ65% of viral genomes were unique to a particular depth. Similarly to Lake A data, a study of Lake Shunet, a sub-Arctic meromictic lake in Siberia (39), showed that very few viral taxa were present throughout the water column. However, in this study, the highest relative viral diversity was observed in the surface stratum.…”

Section: Discussionmentioning

confidence: 81%

Extreme Viral Partitioning in a Marine-Derived High Arctic Lake

Labbé

Girard

Vincent

et al. 2020

mSphere

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High-latitude, perennially stratified (meromictic) lakes are likely to be especially vulnerable to climate warming because of the importance of ice in maintaining their water column structure and associated distribution of microbial communities. This study aimed to characterize viral abundance, diversity, and distribution in a meromictic lake of marine origin on the far northern coast of Ellesmere Island, in the Canadian High Arctic. We collected triplicate samples for double-stranded DNA (dsDNA) viromics from five depths that encompassed the major features of the lake, as determined by limnological profiling of the water column. Viral abundance and virus-to-prokaryote ratios were highest at greater depths, while bacterial and cyanobacterial counts were greatest in the surface waters. The viral communities from each zone of the lake defined by salinity, temperature, and dissolved oxygen concentrations were markedly distinct, suggesting that there was little exchange of viral types among lake strata. Ten viral assembled genomes were obtained from our libraries, and these also segregated with depth. This well-defined structure of viral communities was consistent with that of potential hosts. Viruses from the monimolimnion, a deep layer of ancient Arctic Ocean seawater, were more diverse and relatively abundant, with few similarities to available viral sequences. The Lake A viral communities also differed from published records from the Arctic Ocean and meromictic Ace Lake in Antarctica. This first characterization of viral diversity from this sentinel environment underscores the microbial richness and complexity of an ecosystem type that is increasingly exposed to major perturbations in the fast-changing Arctic. IMPORTANCE The Arctic is warming at an accelerating pace, and the rise in temperature has increasing impacts on the Arctic biome. Lakes are integrators of their surroundings and thus excellent sentinels of environmental change. Despite their importance in the regulation of key microbial processes, viruses remain largely uncharacterized in Arctic lacustrine environments. We sampled a highly stratified meromictic lake near the northern limit of the Canadian High Arctic, a region in rapid transition due to climate change. We found that the different layers of the lake harbored viral communities that were strikingly dissimilar and highly divergent from known viruses. Viruses were more abundant in the deepest part of the lake containing ancient Arctic Ocean seawater that was trapped during glacial retreat and were genomically unlike any viruses previously described. This research demonstrates the complexity and novelty of viral communities in an environment that is vulnerable to ongoing perturbation.

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Section: Discussionmentioning

confidence: 81%

Extreme Viral Partitioning in a Marine-Derived High Arctic Lake

Labbé

Girard

Vincent

et al. 2020

mSphere

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“…M30B3, abbreviated as M30B3. The M30B3 is the predominant bacterium in Lake Shunet at 3.0 m and plays a pivotal role in providing organic carbon in the lake ecosystem [12].…”

Section: Resultsmentioning

confidence: 99%

“…Using comparative genomics, unique and intriguing metabolic features are identified in these complete MAGs, including two predominant novel species: Thiocapsa sp, and Cyanobium sp. [12]. The findings show that it is advantageous to apply this method in studies of microbial ecology and microbial genomics by revising and improving the shortcomings of SRs-based metagenomes.…”

Section: Discussionmentioning

confidence: 99%

“…Our workflow combines Illumina sequencing reads and Nanopore long sequencing reads to recover many novel high-quality and high-contiguity prokaryotic MAGs from Lake Shunet, southern Siberia, one of only four meromictic lakes in all of Siberia. The lake contains stratified water layers, including a mixolimnion layer at 3.0 m, chemocline at 5.0 m, and monimolimnion at 5.5 m. From our previous 16 rRNA amplicon survey, we know that the lake comprises at least hundreds of unknown bacteria and archaea [12], highlighting the importance of mining microbial MAGs from this rarely explored lake. However, though we attempted to recover MAGs from these layers using deep Illumina sequencing with approximately 150 Gb, only one high-quality but still fragmented MAG was obtained [12].…”

Section: Introductionmentioning

confidence: 99%

“…The lake contains stratified water layers, including a mixolimnion layer at 3.0 m, chemocline at 5.0 m, and monimolimnion at 5.5 m. From our previous 16 rRNA amplicon survey, we know that the lake comprises at least hundreds of unknown bacteria and archaea [12], highlighting the importance of mining microbial MAGs from this rarely explored lake. However, though we attempted to recover MAGs from these layers using deep Illumina sequencing with approximately 150 Gb, only one high-quality but still fragmented MAG was obtained [12]. Hence, in this study, we developed a new workflow combining Illumina and Nanopore sequencing reads by integrating several cutting-edge bioinformatics tools to recover and reconstruct MAGs with high contiguity and accuracy.…”

Section: Introductionmentioning

confidence: 99%

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Salvaging complete and high-quality genomes of novel microbial species from a meromictic lake using a workflow combining long- and short-read sequencing platforms

Chen

Chiang

et al. 2021

Preprint

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Background: Most of Earth's bacteria have yet to be cultivated. The metabolic and functional potentials of these uncultivated microorganisms thus remain mysterious, and the metagenome-assembled genome (MAG) approach is the most robust method for uncovering these potentials. However, MAGs discovered by conventional metagenomic assembly and binning methods are usually highly fragmented genomes with heterogeneous sequence contamination, and this affects the accuracy and sensitivity of genomic analyses. Though the maturation of long-read sequencing technologies provides a good opportunity to fix the problem of highly fragmented MAGs as mentioned above, the method's error-prone nature causes severe problems of long-read-alone metagenomics. Hence, methods are urgently needed to retrieve MAGs by a combination of both long- and short-read technologies to advance genome-centric metagenomics. Results: In this study, we combined Illumina and Nanopore data to develop a new workflow to reconstruct 233 MAGs-six novel bacterial orders, 20 families, 66 genera, and 154 species-from Lake Shunet, a secluded meromictic lake in Siberia. Those new MAGs were underrepresented or undetectable in other MAGs studies using metagenomes from human or other common organisms or habitats. Using this newly developed workflow and strategy, the average N50 of reconstructed MAGs greatly increased 10-40-fold compared to when the conventional Illumina assembly and binning method were used. More importantly, six complete MAGs were recovered from our datasets, five of which belong to novel species. We used these as examples to demonstrate many novel and intriguing genomic characteristics discovered in these newly complete genomes and proved the importance of high-quality complete MAGs in microbial genomics and metagenomics studies. Conclusions: The results show that it is feasible to apply our workflow with a few additional long reads to recover numerous complete and high-quality MAGs from short-read metagenomes of high microbial diversity environment samples. The unique features we identified from five complete genomes highlight the robustness of this method in genome-centric metagenomic research. The recovery of 154 novel species MAGs from a rarely explored lake greatly expands the current bacterial genome encyclopedia and broadens our knowledge by adding new genomic characteristics of bacteria. It demonstrates a strong need to recover MAGs from diverse unexplored habitats in the search for microbial dark matter.

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Vertical niche occupation and potential metabolic interplay of microbial consortia in a deeply stratified meromictic model lake

Cabello‐Yeves,

Picazo,

Roda‐Garcia

et al. 2023

Limnology & Oceanography

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The microbial ecology of meromictic lakes assessed with “omics” is still poorly studied compared to other aquatic systems. Here, a combination of metagenomics, high resolution sampling and detailed physical–chemical data gathering allowed to study the planktonic prokaryotic assemblages and metabolic capabilities in the crenogenic meromictic Lake El Tobar (Spain), a model lake for such purposes. This system presents a specific stratification comprising a freshwater layer and a halocline linked to the oxycline, driving to the euxinic hypersaline waters of the deep monimolimnion. The different strata showed a highly diverse and vertically distributed microbiome with their metabolic capacities fitting/influencing the physical–chemical environment. Overall, up to 338 novel genomes were found from metagenome assembled genomes. Picocyanobacteria and methanotrophs were abundant in the upper part of the oxycline. Anoxygenic phototrophs (Chlorobium, Thiohalocapsa, Chromatiaceae, Rhodospirillum, and Rhodobacteraceae spp.) dominated the 12.5–14 m anoxic waters with dim light availability. Sulfate reducers (Desulfobacterota and Firmicutes) inhabited low redox horizons from 13.5 to the bottom (18 m). The potential microbial synergistic performance increases toward the monimolimnion. Among these, a microbial assemblage mostly composed of Spirochaetota, Cloacimonadota, Omitrophota, Firmicutes, Marinisomatota, Nanoarchaeota, and Patescibacteria in hypersaline waters of 14–18 m (conductivities of 118–213 mS cm−1), is potentially capable of performing mixed‐acid fermentations, even including hydrogen and butanol biosynthesis of biotechnological interest. This metagenomics study shows how microbial lifestyles may be determinant in the interplay of environmental gradients, and exemplifies the potential interactions between the microbial guilds thereby.

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Comprehensive Insights Into Composition, Metabolic Potentials, and Interactions Among Archaeal, Bacterial, and Viral Assemblages in Meromictic Lake Shunet in Siberia

Cited by 11 publications

References 100 publications

Extreme Viral Partitioning in a Marine-Derived High Arctic Lake

Extreme Viral Partitioning in a Marine-Derived High Arctic Lake

Salvaging complete and high-quality genomes of novel microbial species from a meromictic lake using a workflow combining long- and short-read sequencing platforms

Vertical niche occupation and potential metabolic interplay of microbial consortia in a deeply stratified meromictic model lake

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