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Metagenomic Features Characterized with Microbial Iron Oxidoreduction and Mineral Interaction in Southwest Indian Ridge.

ABSTRACT: The Southwest Indian Ridge (SWIR) is one of the typical representatives of deep-sea ultraslow-spreading ridges, and has increasingly become a hot spot of studying subsurface geological activities and deep-sea mining management. However, the understanding of microbial activities is still limited on active hydrothermal vent chimneys in SWIR. In this study, samples from an active black smoker and a diffuse vent located in the Longqi hydrothermal region were collected for deep metagenomic sequencing, which yielded approximately 290 GB clean data and 295 mid-to-high-quality metagenome-assembled genomes (MAGs). Sulfur oxidation conducted by a variety of Gammaproteobacteria, Alphaproteobacteria, and Campylobacterota was presumed to be the major energy source for chemosynthesis in Longqi hydrothermal vents. Diverse iron-related microorganisms were recovered, including iron-oxidizing Zetaproteobacteria, iron-reducing Deferrisoma, and magnetotactic bacterium. Twenty-two bacterial MAGs from 12 uncultured phyla harbored iron oxidase Cyc2 homologs and enzymes for organic carbon degradation, indicated novel chemolithoheterotrophic iron-oxidizing bacteria that affected iron biogeochemistry in hydrothermal vents. Meanwhile, potential interactions between microbial communities and chimney minerals were emphasized as enriched metabolic potential of siderophore transportation, and extracellular electron transfer functioned by multi-heme proteins was discovered. Composition of chimney minerals probably affected microbial iron metabolic potential, as pyrrhotite might provide more available iron for microbial communities. Collectively, this study provides novel insights into microbial activities and potential mineral-microorganism interactions in hydrothermal vents. IMPORTANCE Microbial activities and interactions with minerals and venting fluid in active hydrothermal vents remain unclear in the ultraslow-spreading SWIR (Southwest Indian Ridge). Understanding about how minerals influence microbial metabolism is currently limited given the obstacles in cultivating microorganisms with sulfur or iron oxidoreduction functions. Here, comprehensive descriptions on microbial composition and metabolic profile on 2 hydrothermal vents in SWIR were obtained based on cultivation-free metagenome sequencing. In particular, autotrophic sulfur oxidation supported by minerals was presumed, emphasizing the role of chimney minerals in supporting chemosynthesis. Presence of novel heterotrophic iron-oxidizing bacteria was also indicated, suggesting overlooked biogeochemical pathways directed by microorganisms that connected sulfide mineral dissolution and organic carbon degradation in hydrothermal vents. Our findings offer novel insights into microbial function and biotic interactions on minerals in ultraslow-spreading ridges.

SUBMITTER: Zhong YW

PROVIDER: S-EPMC9769843 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Metagenomic Features Characterized with Microbial Iron Oxidoreduction and Mineral Interaction in Southwest Indian Ridge.

Zhong Ying-Wen YW Zhou Peng P Cheng Hong H Zhou Ya-Dong YD Pan Jie J Xu Lin L Li Meng M Tao Chun-Hui CH Wu Yue-Hong YH Xu Xue-Wei XW

Microbiology spectrum 20221026 6

The Southwest Indian Ridge (SWIR) is one of the typical representatives of deep-sea ultraslow-spreading ridges, and has increasingly become a hot spot of studying subsurface geological activities and deep-sea mining management. However, the understanding of microbial activities is still limited on active hydrothermal vent chimneys in SWIR. In this study, samples from an active black smoker and a diffuse vent located in the Longqi hydrothermal region were collected for deep metagenomic sequencing ...[more]

PMID: 36286994

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Project description:UNLABELLED:Sulfur is an important element in sustaining microbial communities present in hydrothermal vents. Sulfur oxidation has been extensively studied due to its importance in chemosynthetic pathways in hydrothermal fields; however, less is known about sulfate reduction. Here, the metagenomes of hydrothermal chimneys located on the ultraslow-spreading Southwest Indian Ridge (SWIR) were pyrosequenced to elucidate the associated microbial sulfur cycle. A taxonomic summary of known genes revealed a few dominant bacteria that participated in the microbial sulfur cycle, particularly sulfate-reducing Deltaproteobacteria. The metagenomes studied contained highly abundant genes related to sulfur oxidation and reduction. Several carbon metabolic pathways, in particular the Calvin-Benson-Bassham pathway and the reductive tricarboxylic acid cycles for CO2 fixation, were identified in sulfur-oxidizing autotrophic bacteria. In contrast, highly abundant genes related to the oxidation of short-chain alkanes were grouped with sulfate-reducing bacteria, suggesting an important role for short-chain alkanes in the sulfur cycle. Furthermore, sulfur-oxidizing bacteria were associated with enrichment for genes involved in the denitrification pathway, while sulfate-reducing bacteria displayed enrichment for genes responsible for hydrogen utilization. In conclusion, this study provides insights regarding major microbial metabolic activities that are driven by the sulfur cycle in low-temperature hydrothermal chimneys present on an ultraslow midocean ridge. IMPORTANCE:There have been limited studies on chimney sulfides located at ultraslow-spreading ridges. The analysis of metagenomes of hydrothermal chimneys on the ultraslow-spreading Southwest Indian Ridge suggests the presence of a microbial sulfur cycle. The sulfur cycle should be centralized within a microbial community that displays enrichment for sulfur metabolism-related genes. The present study elucidated a significant role of the microbial sulfur cycle in sustaining an entire microbial community in low-temperature hydrothermal chimneys on an ultraslow spreading midocean ridge, which has characteristics distinct from those of other types of hydrothermal fields.

Project description:Deep sea microbial communities play a significant role in global biogeochemical processes. However, the depth-wise metabolic potential of microbial communities in hydrothermally influenced Central Indian Ridge (CIR) and Southwest Indian Ridge (SWIR) remains elusive. In this study, a comprehensive functional microarray-based approach was used to understand factors influencing the metabolic potential of microbial communities and depth-driven differences in microbial functional gene composition in CIR and SWIR. Stratified water column sampling at surface, mid, turbid/plume layer, and near bottom was done along with pertinent environmental variables at various locations along the ridges. The majority of genes (~38%-41%) throughout the water column in both regions encoded for C-cycling, particularly starch degradation indicating the predominance of heterotrophy. Genes encoding for nitrate reduction and arsenic and mercury resistance were enriched in the turbid and/or near-bottom waters, suggesting a localized influence of hydrothermally derived substrates on the metabolic potential of microbial communities. Indices for microbial functional gene diversity (H = 9.18) and evenness (J = 0.90) were highest for samples from turbid waters at SWIR. Potential temperature-salinity profiles showed the presence of nutrient-rich upper circumpolar deep water (UCDW) at >2,000 m in the study areas. Principal component analysis revealed that inorganic nutrient availability largely influenced functional gene diversity in deeper waters. The study signifies that rather than hydrothermal input, nutrients brought into the region through the UCDW could have a larger impact on metabolic processes mediated by autochthonous microbial communities and consequently have implications on deep-sea productivity.IMPORTANCELittle is known about depth-wise metabolic potential of microbial communities in hydrothermally influenced Central Indian Ridge (CIR) and Southwest Indian Ridge (SWIR) waters. In the present study, a comprehensive functional gene microarray approach was used to reveal the metabolic potential and depth-wise variation in microbial functional genes along the ridges. Up to 41% of microbial functional genes at both locations encoded for C-cycling. Availability of hydrothermally derived substrates in plumes detected along the ridges triggered an increase in the abundance of genes encoding for remediation of polycyclic aromatics, nitrate reduction, and arsenic and mercury resistance. Rather than hydrothermal input, the functional gene diversity at >2,000 m was largely influenced by inorganic nutrients transported by the nutrient-rich upper circumpolar deep water. Findings of this study are expanding the existing knowledge on new sites of hydrothermal activity along CIR and SWIR and gaining insights into ecosystem functioning in the deep sea.

Project description:International Ocean Discovery Program Expedition 360 drilled Hole U1473A at Atlantis Bank, an oceanic core complex on the Southwest Indian Ridge, with the aim of recovering representative samples of the lower oceanic crust. Recovered cores were primarily gabbro and olivine gabbro. These mineralogies may host serpentinization reactions that have the potential to support microbial life within the recovered rocks or at greater depths beneath Atlantis Bank. We quantified prokaryotic cells and analyzed microbial community composition for rock samples obtained from Hole U1473A and conducted nutrient addition experiments to assess if nutrient supply influences the composition of microbial communities. Microbial abundance was low (≤104 cells cm-3) but positively correlated with the presence of veins in rocks within some depth ranges. Due to the heterogeneous nature of the rocks downhole (alternating stretches of relatively unaltered gabbros and more significantly altered and fractured rocks), the strength of the positive correlations between rock characteristics and microbial abundances was weaker when all depths were considered. Microbial community diversity varied at each depth analyzed. Surprisingly, addition of simple organic acids, ammonium, phosphate, or ammonium plus phosphate in nutrient addition experiments did not affect microbial diversity or methane production in nutrient addition incubation cultures over 60 weeks. The work presented here from Site U1473A, which is representative of basement rock samples at ultraslow spreading ridges and the usually inaccessible lower oceanic crust, increases our understanding of microbial life present in this rarely studied environment and provides an analog for basement below ocean world systems such as Enceladus. IMPORTANCE The lower oceanic crust below the seafloor is one of the most poorly explored habitats on Earth. The rocks from the Southwest Indian Ridge (SWIR) are similar to rock environments on other ocean-bearing planets and moons. Studying this environment helps us increase our understanding of life in other subsurface rocky environments in our solar system that we do not yet have the capability to access. During an expedition to the SWIR, we drilled 780 m into lower oceanic crust and collected over 50 rock samples to count the number of resident microbes and determine who they are. We also selected some of these rocks for an experiment where we provided them with different nutrients to explore energy and carbon sources preferred for growth. We found that the number of resident microbes and community structure varied with depth. Additionally, added nutrients did not shape the microbial diversity in a predictable manner.

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Metagenomic Features Characterized with Microbial Iron Oxidoreduction and Mineral Interaction in Southwest Indian Ridge.

Publications

Metagenomic Features Characterized with Microbial Iron Oxidoreduction and Mineral Interaction in Southwest Indian Ridge.

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