Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits

Abstract

Background When deep-sea hydrothermal fluids mix with cold oxygenated fluids, minerals precipitate out of solution and form hydrothermal deposits. These actively venting deep-sea hydrothermal deposits support a rich diversity of thermophilic microorganisms which are involved in a range of carbon, sulfur, nitrogen, and hydrogen metabolisms. Global patterns of thermophilic microbial diversity in deep-sea hydrothermal ecosystems have illustrated the strong connectivity between geological processes and microbial colonization, but little is known about the genomic diversity and physiological potential of these novel taxa. Here we explore this genomic diversity in 42 metagenomes from four deep-sea hydrothermal vent fields and a deep-sea volcano collected from 2004 to 2018 and document their potential implications in biogeochemical cycles. Results Our dataset represents 3635 metagenome-assembled genomes encompassing 511 novel and recently identified genera from deep-sea hydrothermal settings. Some of the novel bacterial (107) and archaeal genera (30) that were recently reported from the deep-sea Brothers volcano were also detected at the deep-sea hydrothermal vent fields, while 99 bacterial and 54 archaeal genera were endemic to the deep-sea Brothers volcano deposits. We report some of the first examples of medium- (≥ 50% complete, ≤ 10% contaminated) to high-quality (> 90% complete, < 5% contaminated) MAGs from phyla and families never previously identified, or poorly sampled, from deep-sea hydrothermal environments. We greatly expand the novel diversity of Thermoproteia, Patescibacteria (Candidate Phyla Radiation, CPR), and Chloroflexota found at deep-sea hydrothermal vents and identify a small sampling of two potentially novel phyla, designated JALSQH01 and JALWCF01. Metabolic pathway analysis of metagenomes provides insights into the prevalent carbon, nitrogen, sulfur, and hydrogen metabolic processes across all sites and illustrates sulfur and nitrogen metabolic “handoffs” in community interactions. We confirm that Campylobacteria and Gammaproteobacteria occupy similar ecological guilds but their prevalence in a particular site is driven by shifts in the geochemical environment. Conclusion Our study of globally distributed hydrothermal vent deposits provides a significant expansion of microbial genomic diversity associated with hydrothermal vent deposits and highlights the metabolic adaptation of taxonomic guilds. Collectively, our results illustrate the importance of comparative biodiversity studies in establishing patterns of shared phylogenetic diversity and physiological ecology, while providing many targets for enrichment and cultivation of novel and endemic taxa.

Metagenomics reveals the habitat specificity of biosynthetic potential of secondary metabolites in global food fermentations

“…Meanwhile, MAG quality cutoff would also be responsible for the MAGs discrepancies. The MAG quality cutoff was ≥ 50% completeness and ≤ 10% contamination in this study, which was in line with previous studies [ 54 , 55 ]. In reported cocoa and cheese fermentation samples, the MAG quality cutoff were ≥ 50% completeness and < 10% contamination [ 34 ] and ≥ 80% completeness and ≤ 10% contamination [ 21 ], respectively.…”

The trade-off between individual metabolic specialization and versatility determines the metabolic efficiency of microbial communities

“…Our genomic analysis suggests that such a form of "partial redundancy" is prevalent in the community performing hydrocarbon degradation. Previous metagenomic studies also observed similar phenomena in the degradation of other organic compounds 42 , as well as other metabolic activities, such as sulfur oxidation, denitrification, and sulfate reduction 53 . As an optimal level of redundancy can enhance the function of a community, it can be assumed that those communities which maintain an adequate level of functional redundancy are likely to be favored selectively in nature, especially when environmental pressures act on communities with higher function (for instance, a community-consuming substrate and accumulating biomass at a faster rate).…”

Viromes vs. mixed community metagenomes: choice of method dictates interpretation of viral community ecology

“…While this exception may be influenced by the smaller filter size used to sample marine viromes compared to those used to generate the other datasets used here, the environments from which marine samples were collected are perhaps the most distinguished out of the others owing to their origin from hydrothermal vent plumes in the deep sea. These environments have been shown to be composed of ultra-small microbes that can have cell sizes <0.22 μm [69,70,76–78], requiring modified virome extraction methods, just as the other environmental sources here require in other respects [64,65].…”