High-Throughput Sequencing Reveals a Potentially Novel Sulfurovum Species Dominating the Microbial Communities of the Seawater-Sediment Interface of a Deep-Sea Cold Seep in South China Sea.
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ABSTRACT:
SUBMITTER: Sun QL
PROVIDER: S-EPMC7284658 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Chemoautotrophs within Campylobacterota, especially Sulfurovum and Sulfurimonas, are abundant in the seawater-sediment interface of the Formosa cold seep in the South China Sea. However, the in situ activity and function of Campylobacterota are unknown. In this study, the geochemical role of Campylobacterota in the Formosa cold seep was investigated with multiple means. Two members of Sulfurovum and Sulfurimonas were isolated for the first time from deep-sea cold seep. These isolates are new chemoautotrophic species that can use molecular hydrogen as an energy source and CO2 as a sole carbon source. Comparative genomics identified an important hydrogen-oxidizing cluster in Sulfurovum and Sulfurimonas. Metatranscriptomic analysis detected high expression of hydrogen-oxidizing gene in the RS, suggesting that H2 was likely an energy source in the cold seep. Genomic analysis indicated that the Sulfurovum and Sulfurimonas isolates possess a truncated sulfur-oxidizing system, and metatranscriptomic analysis revealed that Sulfurovum and Sulfurimonas with this genotype were active in the surface of RS and likely contributed to thiosulfate production. Furthermore, geochemical and in situ analyses revealed sharply decreased nitrate concentration in the sediment-water interface due to microbial consumption. Consistently, the denitrification genes of Sulfurimonas and Sulfurovum were highly expressed, suggesting an important contribution of these bacteria to nitrogen cycling. Overall, this study demonstrated that Campylobacterota played a significant role in the cycling of nitrogen and sulfur in a deep-sea cold seep. IMPORTANCE Chemoautotrophs within Campylobacterota, in particular Sulfurovum and Sulfurimonas, are ubiquitous in deep-sea cold seeps and hydrothermal vents. However, to date, no Sulfurovum or Sulfurimonas has been isolated from cold seeps, and the ecological roles of these bacteria in cold seeps remain to be investigated. In this study, we obtained two isolates of Sulfurovum and Sulfurimonas from Formosa cold seep, South China Sea. Comparative genomics, metatranscriptomics, geochemical analysis, and in situ experimental study indicated collectively that Campylobacterota played a significant part in nitrogen and sulfur cycling in cold seep and was the cause of thiosulfate accumulation and sharp reduction of nitrate level in the sediment-water interface. The findings of this study promoted our understanding of the in situ function and ecological role of deep-sea Campylobacterota.
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Project description:Benefiting from the rapid developments and wide applications of high-throughput sequencing, great advancements have been made in investigating microbiota, which are highly diverse and play key roles in both element cycling and the energy flow of ecosystems. There have been inherent limitations of amplicon sequencing that could introduce uncertainty and raise concerns about the accuracy and reproducibility of this technology. However, studies focusing on the reproducibility of amplicon sequencing are limited, especially in characterizing microbial communities in deep-sea sediments. To evaluate reproducibility, 118 deep-sea sediment samples were used for 16S rRNA gene sequencing in technical replicates (repeated measurements of the same sample) that demonstrate the variability of amplicon sequencing. The average occurrence-based overlaps were 35.98% and 27.02% between two and among three technical replicates, respectively, whereas their abundance-based overlaps reached 84.88% and 83.16%, respectively. Although variations of alpha and beta diversity indices were found between/among technical replicates, alpha diversity indices were similar across samples, and the average beta diversity indices were much smaller for technical replicates than among samples. Moreover, clustering methods (i.e., operational taxonomic units [OTUs] and amplicon sequence variants [ASVs]) were shown to have little impact on the alpha and beta diversity patterns of microbial communities. Taken together, although there are variations between/among technical replicates, amplicon sequencing is still a powerful tool with which to reveal diversity patterns of microbiota in deep-sea sediments. IMPORTANCE The reproducibility of amplicon sequencing is vital for whether the diversities of microbial communities could be accurately estimated. Thus, reproducibility influences the drawing of sound ecological conclusions. Nevertheless, few studies have focused on the reproducibility of microbial communities that are characterized by amplicon sequencing, and studies focusing on microbiota in deep-sea sediments have been especially lacking. In this study, we evaluated the reproducibility of amplicon sequencing targeting microbiota in deep-sea sediments of cold seep. Our results revealed that there were variations between/among technical replicates and that amplicon sequencing was still a powerful tool with which to characterize the diversities of microbial communities in deep-sea sediments. This study provides valuable guidelines for the reproducibility evaluation of future work in experimental design and interpretation.
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Project description:Cold seeps are biological oases of the deep sea fueled by methane, sulfates, nitrates, and other inorganic sources of energy. Chemolithoautotrophic bacteria and archaea dominate seep sediment, and their diversity and biogeochemical functions are well established. Fungi are likewise diverse, metabolically versatile, and known for their ability to capture and oxidize methane. Still, no study has ever explored the functional role of the mycobiota in the cold seep biome. To assess the complex role of fungi and fill in the gaps, we performed network analysis on 147 samples to disentangle fungal-prokaryotic interactions (fungal 18S and prokaryotic 16S) in the Haima cold seep region. We demonstrated that fungi are central species with high connectivity at the epicenter of prokaryotic networks, reduce their random-attack vulnerability by 60%, and enhance information transfer efficiency by 15%. We then scavenged a global metagenomic and metatranscriptomic data set from 10 cold seep regions for fungal genes of interest (hydrophobins, cytochrome P450s, and ligninolytic family of enzymes); this is the first study to report active transcription of 2,500+ fungal genes in the cold seep sediment. The genera Fusarium and Moniliella were of notable importance and directly correlated with high methane abundance in the sulfate-methane transition zone (SMTZ), likely due to their ability to degrade and solubilize methane and oils. Overall, our results highlight the essential yet overlooked contribution of fungi to cold seep biological networks and the role of fungi in regulating cold seep biogeochemistry. IMPORTANCE The challenges we face when analyzing eukaryotic metagenomic and metatranscriptomic data sets have hindered our understanding of cold seep fungi and microbial eukaryotes. This fact does not make the mycobiota any less critical in mediating cold seep biogeochemistry. On the contrary, many fungal genera can oxidize and solubilize methane, produce methane, and play a unique role in nutrient recycling via saprotrophic enzymatic activity. In this study, we used network analysis to uncover key fungal-prokaryotic interactions that can mediate methane biogeochemistry and metagenomics and metatranscriptomics to report that fungi are transcriptionally active in the cold seep sediment. With concerns over rising methane levels and cold seeps being a pivotal source of global methane input, our holistic understanding of methane biogeochemistry with all domains of life is essential. We ultimately encourage scientists to utilize state-of-the-art tools and multifaceted approaches to uncover the role of microeukaryotic organisms in understudied systems.
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Project description:Bathymodiolid mussels dominate hydrothermal vents, cold methane/sulfide-hydrocarbon seeps, and other sites of organic enrichment. Here, we aimed to explore the innate immune system and detoxification mechanism of the deep sea mussel Bathymodiolus platifrons collected from a methane seep in the South China Sea. We sequenced the transcriptome of the mussels' gill, foot and mantle tissues and generated a transcriptomic database containing 96,683 transcript sequences. Based on GO and KEGG annotations, we reported transcripts that were related to the innate immune system, heavy metal detoxification and sulfide metabolic genes. Our in-depth analysis on the isoforms of peptidoglycan recognition protein (PGRP) that have different cellular location and potentially differential selectivity towards peptidoglycan (PGN) from gram-positive and gram-negative bacteria were differentially expressed in different tissues. We also reported a potentially novel form of metallothionein and the production of phytochelatin in B. platifrons, which has not been reported in any of its coastal relative Mytilus mussel species. Overall, the present study provided new insights into heavy metal and sulfide metabolism in B. platifrons and can be served as the basis for future molecular studies on host-symbiont interactions in cold seep mussels.
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Project description:Cold seep microbial communities are fascinating ecosystems on Earth which provide unique models for understanding the living strategies in deep-sea distinct environments. In this study, 23 metagenomes were generated from samples collected in the Site-F cold seep field in South China Sea, including the sea water closely above the invertebrate communities, the cold seep fluids, the fluids under the invertebrate communities and the sediment column around the seep vent. By binning tools, we retrieved a total of 768 metagenome assembled genome (MAGs) that were estimated to be >60% complete. Of the MAGs, 61 were estimated to be >90% complete, while an additional 105 were >80% complete. Phylogenomic analysis revealed 597 bacterial and 171 archaeal MAGs, of which nearly all were distantly related to known cultivated isolates. In the 768 MAGs, the abundant Bacteria in phylum level included Proteobacteria, Desulfobacterota, Bacteroidota, Patescibacteria and Chloroflexota, while the abundant Archaea included Asgardarchaeota, Thermoplasmatota, and Thermoproteota. These results provide a dataset available for further interrogation of deep-sea microbial ecology.
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