Dataset Information

Coupled Carbon, Sulfur, and Nitrogen Cycles Mediated by Microorganisms in the Water Column of a Shallow-Water Hydrothermal Ecosystem.

ABSTRACT: Shallow-water hydrothermal vent ecosystems are distinctly different from deep-sea vents, as other than geothermal, sunlight is one of their primary sources of energy, so their resulting microbial communities differ to some extent. Yet compared with deep-sea systems, less is known about the active microbial community in shallow-water ecosystems. Thus, we studied the community compositions, their metabolic pathways, and possible coupling of microbially driven biogeochemical cycles in a shallow-water hydrothermal vent system off Kueishantao Islet, Taiwan, using high-throughput 16S rRNA sequences and metatranscriptome analyses. Gammaproteobacteria and Epsilonbacteraeota were the major active bacterial groups in the 16S rRNA libraries and the metatranscriptomes, and involved in the carbon, sulfur, and nitrogen metabolic pathways. As core players, Thiomicrospira, Thiomicrorhabdus, Thiothrix, Sulfurovum, and Arcobacter derived energy from the oxidation of reduced sulfur compounds and fixed dissolved inorganic carbon (DIC) by the Calvin-Benson-Bassham (CBB) or reverse tricarboxylic acid cycles. Sox-dependent and reverse sulfate reduction were the main pathways of energy generation, and probably coupled to denitrification by providing electrons to nitrate and nitrite. Sulfur-reducing Nautiliaceae members, accounting for a small proportion in the community, obtained energy by the oxidation of hydrogen, which also supplies metabolic energy for some sulfur-oxidizing bacteria. In addition, ammonia and nitrite oxidation is another type of energy generation in this hydrothermal system, with marker gene sequences belonging to Thaumarchaeota/Crenarchaeota and Nitrospina, respectively, and ammonia and nitrite oxidation was likely coupled to denitrification by providing substrate for nitrate and nitrite reduction to nitric oxide. Moreover, unlike the deep-sea systems, cyanobacteria may also actively participate in major metabolic pathways. This study helps us to better understand biogeochemical processes mediated by microorganisms and possible coupling of the carbon, sulfur, and nitrogen cycles in these unique ecosystems.

SUBMITTER: Li Y

PROVIDER: S-EPMC6282030 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Coupled Carbon, Sulfur, and Nitrogen Cycles Mediated by Microorganisms in the Water Column of a Shallow-Water Hydrothermal Ecosystem.

Li Yufang Y Tang Kai K Zhang Lianbao L Zhao Zihao Z Xie Xiabing X Chen Chen-Tung Arthur CA Wang Deli D Jiao Nianzhi N Zhang Yao Y

Frontiers in microbiology 20181113

Shallow-water hydrothermal vent ecosystems are distinctly different from deep-sea vents, as other than geothermal, sunlight is one of their primary sources of energy, so their resulting microbial communities differ to some extent. Yet compared with deep-sea systems, less is known about the active microbial community in shallow-water ecosystems. Thus, we studied the community compositions, their metabolic pathways, and possible coupling of microbially driven biogeochemical cycles in a shallow-wat ...[more]

PMID: 30555427

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Project description:Hydrothermal vent (HTV) systems are important habitats for understanding the biological processes of extremophiles on Earth and their relative contributions to material and energy cycles in the ocean. Current understanding on hydrothermal systems have been primarily focused on deep-sea HTVs, and little is known about the functions and metabolisms of microorganisms in shallow-water HTVs (SW-HTVs), which are distinguished from deep-sea HTVs by a depth limit of 200 m. In this study, we analyzed metagenomes of sulfur-rich sediment samples collected from a SW-HTV of Kueishan Island, located in a marginal sea of the western Pacific Ocean. Comparing with a previously published report of pelagic samples from the nearby sampling site, microbial communities in the SW-HTV sediments enriching with genes of both aerobic and anaerobic respiration inferred variable environments in the tested sediments. Abundant genes of energy metabolism encoding sulfur oxidation, H2 oxidation, and carbon fixation were detected from the sediment samples. Sixty-eight metagenome-assembled-genomes (MAGs) were reconstructed to further understand the metabolism and potential interactions between different microbial taxa in the SW-HTVs sediment. MAGs with the highest abundant were chemolithotrophic sulfur-oxidization bacteria, including Sulfurovum represented Campylobacteria involved sox multienzyme, sulfide oxidation genes and rTCA cycle, and Gammaproteobacteria involved dsr gene and CBB cycle. In addition, Desulfobacterota with the potential to participate in sulfur-disproportionating processes also had higher abundance than the sample's overall mean value. The interaction of these bacterial groups allows the microbial communities to efficiently metabolize a large variety of sulfur compounds. In addition, the potential to use simple organic carbon, such as acetate, was found in chemolithotrophic Campylobacterial MAGs. Collectively, our results revealed the complexity of environmental conditions of the vent sediment and highlight the interactive relationships of the dominant microbial populations in driving sulfur cycles in the SW-HTV sediments off Kueishan Island.

Project description:BackgroundActive hydrothermal vents create extreme conditions characterized by high temperatures, low pH levels, and elevated concentrations of heavy metals and other trace elements. These conditions support unique ecosystems where chemolithoautotrophs serve as primary producers. The steep temperature and pH gradients from the vent mouth to its periphery provide a wide range of microhabitats for these specialized microorganisms. However, their metabolic functions, adaptations in response to these gradients, and coping mechanisms under extreme conditions remain areas of limited knowledge. In this study, we conducted temperature gradient incubations of hydrothermal fluids from moderate (pH = 5.6) and extremely (pH = 2.2) acidic vents. Combining the DNA-stable isotope probing technique and subsequent metagenomics, we identified active chemolithoautotrophs under different temperature and pH conditions and analyzed their specific metabolic mechanisms.ResultsWe found that the carbon fixation activities of Nautiliales in vent fluids were significantly increased from 45 to 65 °C under moderately acidic condition, while their heat tolerance was reduced under extremely acidic conditions. In contrast, Campylobacterales actively fixed carbon under both moderately and extremely acidic conditions under 30 - 45 °C. Compared to Campylobacterales, Nautiliales were found to lack the Sox sulfur oxidation system and instead use NAD(H)-linked glutamate dehydrogenase to boost the reverse tricarboxylic acid (rTCA) cycle. Additionally, they exhibit a high genetic potential for high activity of cytochrome bd ubiquinol oxidase in oxygen respiration and hydrogen oxidation at high temperatures. In terms of high-temperature adaption, the rgy gene plays a critical role in Nautiliales by maintaining DNA stability at high temperature. Genes encoding proteins involved in proton export, including the membrane arm subunits of proton-pumping NADH: ubiquinone oxidoreductase, K+ accumulation, selective transport of charged molecules, permease regulation, and formation of the permeability barrier of bacterial outer membranes, play essential roles in enabling Campylobacterales to adapt to extremely acidic conditions.ConclusionsOur study provides in-depth insights into how high temperature and low pH impact the metabolic processes of energy and main elements in chemolithoautotrophs living in hydrothermal ecosystems, as well as the mechanisms they use to adapt to the extreme hydrothermal conditions. Video Abstract.

Dataset Information

Coupled Carbon, Sulfur, and Nitrogen Cycles Mediated by Microorganisms in the Water Column of a Shallow-Water Hydrothermal Ecosystem.

Publications

Coupled Carbon, Sulfur, and Nitrogen Cycles Mediated by Microorganisms in the Water Column of a Shallow-Water Hydrothermal Ecosystem.

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