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Genome-resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep-sea hydrothermal vents.

ABSTRACT: The structure and function of microbial communities inhabiting the subseafloor near hydrothermal systems are influenced by fluid geochemistry, geologic setting and fluid flux between vent sites, as well as biological interactions. Here, we used genome-resolved metagenomics and metatranscriptomics to examine patterns of gene abundance and expression and assess potential niche differentiation in microbial communities in venting fluids from hydrothermal vent sites at the Mid-Cayman Rise. We observed similar patterns in gene and transcript abundance between two geochemically distinct vent fields at the community level but found that each vent site harbours a distinct microbial community with differing transcript abundances for individual microbial populations. Through an analysis of metabolic pathways in 64 metagenome-assembled genomes (MAGs), we show that MAG transcript abundance can be tied to differences in metabolic pathways and to potential metabolic interactions between microbial populations, allowing for niche-partitioning and divergence in both population distribution and activity. Our results illustrate that most microbial populations have a restricted distribution within the seafloor, and that the activity of those microbial populations is tied to both genome content and abiotic factors.

SUBMITTER: Galambos D

PROVIDER: S-EPMC6899741 | biostudies-literature | 2019 Nov

REPOSITORIES: biostudies-literature

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Genome-resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep-sea hydrothermal vents.

Galambos David D Anderson Rika E RE Reveillaud Julie J Huber Julie A JA

Environmental microbiology 20191017 11

The structure and function of microbial communities inhabiting the subseafloor near hydrothermal systems are influenced by fluid geochemistry, geologic setting and fluid flux between vent sites, as well as biological interactions. Here, we used genome-resolved metagenomics and metatranscriptomics to examine patterns of gene abundance and expression and assess potential niche differentiation in microbial communities in venting fluids from hydrothermal vent sites at the Mid-Cayman Rise. We observe ...[more]

PMID: 31573126

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Project description:BackgroundDeep-sea hydrothermal vents represent unique ecosystems that redefine our understanding of the limits of life. They are widely distributed in deep oceans and typically form along mid-ocean ridges. To date, the hydrothermal systems in the Mid-Atlantic Ridge south of 14°S remain barely explored, limiting our understanding of the microbial community in this distinct ecosystem. The Deyin-1 is a newly discovered hydrothermal field in this area. By applying the metagenomic analysis, we aim at gaining much knowledge of the biodiversity and functional capability of microbial community inhabiting this field.ResultsIn the current study, 219 metagenomic assembled genomes (MAGs) were reconstructed, unveiling a diverse and variable community dominated by Bacteroidetes, Nitrospirae, Alpha-, Delta-, and Gammaproteobacteria in the active and inactive chimney samples as well as hydrothermal oxide samples. Most of these major taxa were potentially capable of using reduced sulfur and hydrogen as primary energy sources. Many members within the major taxa exhibited potentials of metabolic plasticity by possessing multiple energy metabolic pathways. Among these samples, different bacteria were found to be the major players of the same metabolic pathways, further supporting the variable and functionally redundant community in situ. In addition, a high proportion of MAGs harbored the genes of carbon fixation and extracellular carbohydrate-active enzymes, suggesting that both heterotrophic and autotrophic strategies could be essential for their survival. Notably, for the first time, the genus Candidatus Magnetobacterium was shown to potentially fix nitrogen, indicating its important role in the nitrogen cycle of inactive chimneys. Moreover, the metabolic plasticity of microbes, diverse and variable community composition, and functional redundancy of microbial communities may represent the adaptation strategies to the geochemically complex and fluctuating environmental conditions in deep-sea hydrothermal fields.ConclusionsThis represents the first assembled-genome-based investigation into the microbial community and metabolism of a hydrothermal field in the Mid-Atlantic Ridge south of 14°S. The findings revealed that a high proportion of microbes could benefit from simultaneous use of heterotrophic and autotrophic strategies in situ. It also presented novel members of potential diazotrophs and highlighted the metabolic plasticity and functional redundancy across deep-sea hydrothermal systems. Video abstract.

Project description:Deep-sea hydrothermal vent chimneys harbor a high diversity of largely unknown microorganisms. Although the phylogenetic diversity of these microorganisms has been described previously, the adaptation and metabolic potential of the microbial communities is only beginning to be revealed. A pyrosequencing approach was used to directly obtain sequences from a fosmid library constructed from a black smoker chimney 4143-1 in the Mothra hydrothermal vent field at the Juan de Fuca Ridge. A total of 308,034 reads with an average sequence length of 227 bp were generated. Comparative genomic analyses of metagenomes from a variety of environments by two-way clustering of samples and functional gene categories demonstrated that the 4143-1 metagenome clustered most closely with that from a carbonate chimney from Lost City. Both are highly enriched in genes for mismatch repair and homologous recombination, suggesting that the microbial communities have evolved extensive DNA repair systems to cope with the extreme conditions that have potential deleterious effects on the genomes. As previously reported for the Lost City microbiome, the metagenome of chimney 4143-1 exhibited a high proportion of transposases, implying that horizontal gene transfer may be a common occurrence in the deep-sea vent chimney biosphere. In addition, genes for chemotaxis and flagellar assembly were highly enriched in the chimney metagenomes, reflecting the adaptation of the organisms to the highly dynamic conditions present within the chimney walls. Reconstruction of the metabolic pathways revealed that the microbial community in the wall of chimney 4143-1 was mainly fueled by sulfur oxidation, putatively coupled to nitrate reduction to perform inorganic carbon fixation through the Calvin-Benson-Bassham cycle. On the basis of the genomic organization of the key genes of the carbon fixation and sulfur oxidation pathways contained in the large genomic fragments, both obligate and facultative autotrophs appear to be present and contribute to biomass production.

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Genome-resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep-sea hydrothermal vents.

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Genome-resolved metagenomics and metatranscriptomics reveal niche differentiation in functionally redundant microbial communities at deep-sea hydrothermal vents.

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