Dataset Information

Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment.

ABSTRACT: Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as Hydrothermarchaeota) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) from a black smoker chimney and the surrounding sulfur-rich sediments on the South Atlantic Mid-Ocean Ridge and publicly available data sets (the Integrated Microbial Genomes system of the U.S. Department of Energy-Joint Genome Institute and NCBI SRA data sets). Genomic analysis suggested a wide carbon metabolic diversity of Hydrothermarchaeota members, including the utilization of proteins, lactate, and acetate; the anaerobic degradation of aromatics; the oxidation of C1 compounds (CO, formate, and formaldehyde); the utilization of methyl compounds; CO2 incorporation by the tetrahydromethanopterin-based Wood-Ljungdahl pathway; and participation in the type III ribulose-1,5-bisphosphate carboxylase/oxygenase-based Calvin-Benson-Bassham cycle. These microbes also potentially oxidize sulfur, arsenic, and hydrogen and engage in anaerobic respiration based on sulfate reduction and denitrification. Among the 140 MAGs reconstructed from the black smoker chimney microbial community (including Hydrothermarchaeota MAGs), community-level metabolic predictions suggested a redundancy of carbon utilization and element cycling functions and interactive syntrophic and sequential utilization of substrates. These processes might make various carbon and energy sources widely accessible to the microorganisms. Further, the analysis suggested that Hydrothermarchaeota members contained important functional components obtained from the community via lateral gene transfer, becoming a distinctive clade. This might serve as a niche-adaptive strategy for metabolizing heavy metals, C1 compounds, and reduced sulfur compounds. Collectively, the analysis provides comprehensive metabolic insights into the Hydrothermarchaeota IMPORTANCE This study provides comprehensive metabolic insights into the Hydrothermarchaeota from comparative genomics, evolution, and community-level perspectives. Members of the Hydrothermarchaeota synergistically participate in a wide range of carbon-utilizing and element cycling processes with other microorganisms in the community. We expand the current understanding of community interactions within the hydrothermal sediment and chimney, suggesting that microbial interactions based on sequential substrate metabolism are essential to nutrient and element cycling.

SUBMITTER: Zhou Z

PROVIDER: S-EPMC6946796 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of <i>Hydrothermarchaeota</i> in Hydrothermal Sediment.

Zhou Zhichao Z Liu Yang Y Xu Wei W Pan Jie J Luo Zhu-Hua ZH Li Meng M

mSystems 20200107 1

Hydrothermal vents release reduced compounds and small organic carbon compounds into the surrounding seawater, providing essential substrates for microbial growth and bioenergy transformations. Despite the wide distribution of the marine benthic group E archaea (referred to as <i>Hydrothermarchaeota</i>) in the hydrothermal environment, little is known about their genomic repertoires and biogeochemical significance. Here, we studied four highly complete (>80%) metagenome-assembled genomes (MAGs) ...[more]

PMID: 31911466

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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:Deep-sea hydrothermal vents are hotspots for productivity and biodiversity. Thermal pyrolysis and circulation produce fluids rich in hydrocarbons and reduced compounds that stimulate microbial activity in surrounding sediments. Several studies have characterized the diversity of Guaymas Basin (Gulf of California) sediment-inhabiting microorganisms; however, many of the identified taxa lack cultures or genomic representations. Here, we resolved the metabolic potential and community-level interactions of these diverse communities by reconstructing and analyzing microbial genomes from metagenomic sequencing data.We reconstructed 115 microbial metagenome-assembled genomes comprising 27 distinct archaeal and bacterial phyla. The archaea included members of the DPANN and TACK superphyla, Bathyarchaeota, novel Methanosarcinales (GoM-Arc1), and anaerobic methane-oxidizing lineages (ANME-1). Among the bacterial phyla, members of the Bacteroidetes, Chloroflexi, and Deltaproteobacteria were metabolically versatile and harbored potential pathways for hydrocarbon and lipid degradation and a variety of respiratory processes. Genes encoding enzymes that activate anaerobic hydrocarbons for degradation were detected in Bacteroidetes, Chloroflexi, Latescibacteria, and KSB1 phyla, while the reconstructed genomes for most candidate bacteria phyla (Aminicenantes, Atribacteria, Omnitrophica, and Stahlbacteria) indicated a fermentative metabolism. Newly obtained GoM-Arc1 archaeal genomes encoded novel pathways for short-chain hydrocarbon oxidation by alkyl-coenzyme M formation. We propose metabolic linkages among different functional groups, such as fermentative community members sharing substrate-level interdependencies with sulfur- and nitrogen-cycling microbes.Overall, inferring the physiologies of archaea and bacteria from metagenome-assembled genomes in hydrothermal deep-sea sediments has revealed potential mechanisms of carbon cycling in deep-sea sediments. Our results further suggest a network of biogeochemical interdependencies in organic matter utilization, hydrocarbon degradation, and respiratory sulfur cycling among deep-sea-inhabiting microbial communities.

Dataset Information

Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of Hydrothermarchaeota in Hydrothermal Sediment.

Publications

Genome- and Community-Level Interaction Insights into Carbon Utilization and Element Cycling Functions of <i>Hydrothermarchaeota</i> in Hydrothermal Sediment.

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