Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments

Zhang, Chuwen; Shi, Ling-Dong; Li, Jiwei; Xiao, Xu; Shao, Zongze; Dong, Xiyang

doi:10.1038/s41522-023-00382-8

Cited by 5 publications

(4 citation statements)

References 78 publications

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“…Sulfate reduction and anaerobic methane oxidation, associated with dsrA and mcrA gene activities, respectively, are two important metabolic processes in cold seeps 43, 44 . The observed positive correlation between the abundances of rdhA and dsrA genes indicates that reductive dehalogenation and sulfate reduction processes likely occur simultaneously in cold seeps ( Fig.…”

Section: Resultsmentioning

confidence: 99%

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Phylogenetically and structurally diverse reductive dehalogenases link biogeochemical cycles in deep-sea cold seeps

Han,

Peng,

Peng

et al. 2024

Preprint

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Reductive dehalogenation is crucial for halogen cycling and environmental remediation, yet its ecological role is incompletely understood, especially in deep-sea environments. To address this gap, we investigated the diversity of reductive dehalogenases (RDases) and ecophysiology of organohalide reducers in deep-sea cold seeps, which are environments rich in halogenated compounds. Through genome-resolved metagenomic analysis 165 global cold seep sediment samples, we identified four types of RDases, namely prototypical respiratory, transmembrane respiratory, and cytosolic RDases, and one novel clade. These RDases are encoded by physiologically diverse microbes across four archaeal and 36 bacterial phyla, significantly broadening the known diversity of organohalide reducers. Halogen geochemistry, metatranscriptomic data, and metabolomic profiling confirm that organohalides occur at as high as 18 mg/g in these sediments and are actively reduced by microorganisms. This process is tightly linked to other biogeochemical cycles, including carbon, hydrogen, nitrogen, sulfur, and trace elements. RDases from cold seeps have diverse N-terminal structures across different gene groups, and rdhA genes in these environments are mostly functionally constrained and conserved. Altogether, these findings suggest that reductive dehalogenation is a central rather than supplemental process in deep-sea environments, mediated by numerous diverse microbes and novel enzymes.

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Section: Resultsmentioning

confidence: 99%

“…Sulfate reduction and anaerobic methane oxidation, associated with dsrA and mcrA gene activities, respectively, are two important metabolic processes in cold seeps 43,44 .…”

Section: Cold Seeps Harbor a Vast Repertoire Of Reductive Dehalogenas...mentioning

confidence: 99%

Phylogenetically and structurally diverse reductive dehalogenases link biogeochemical cycles in deep-sea cold seeps

Han,

Peng,

Peng

et al. 2024

Preprint

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“…These sites are as follows: Eastern Gulf of Mexico (EGM), Northwestern Gulf of Mexico (GOM), Scotian Basin (SB), Haima seep (HM1, HM3, HM5, S11, SY5, SY6), Haiyang4 (HY4), Site F cold seep (SF), Qiongdongnan Basin (QDN), Shenhu area (SH), and Jiaolong cold seep (JL). Detailed descriptions of the sampling sites and sequencing information for the metagenomic and metatranscriptomic data can be found in our previous work 7,45,58,80 . Paired-end raw reads were quality-controlled by trimming primers and adapters and filtering out artifacts and low-quality reads using the Read_QC module within the metaWRAP pipeline (v1.3.2; -skip-bmtagger) 81 .…”

Section: Collection Of Metagenomes Metatranscriptomes and Magsmentioning

confidence: 99%

A vast repertoire of secondary metabolites influences community dynamics and biogeochemical processes in cold seeps

Dong¹,

Zhang

et al. 2023

Preprint

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In deep sea cold seeps, diverse microbial communities thrive on the geological seepage of hydrocarbons and inorganic compounds. These chemosynthetically-driven communities are unique in composition, ecology, and biogeochemical activities compared to photosynthetically-driven ecosystems. However, their biosynthetic capabilities remain largely unexplored. Here, we analyzed 81 metagenomes, 33 metatranscriptomes, and seven metabolomes derived from nine globally distributed areas of cold seeps to investigate the secondary metabolites produced by cold seep microbiomes. Cold seep microbiomes encode diverse, abundant, and novel biosynthetic gene clusters (BGCs). Most BGCs are affiliated with understudied bacteria and archaea, including key mediators of methane and sulfur cycling, and multiple candidate phyla. The BGCs encode diverse antimicrobial compounds (e.g. NRPS, PKSs, RiPPs) that potentially shape community dynamics, as well as compounds predicted to influence biogeochemical cycling, such as phosphonates, iron-acquiring siderophores, nitrogenase-protecting glycolipids, and methyl-CoM reductase-modifying proteins. BGCs from key players in cold seeps are widely distributed and highly expressed, with their abundance and expression levels varying with different sediment depths. Numerous unique natural products were detected through untargeted sediment metabolomics, demonstrating a vast, unexplored chemical space and validating in situ expression of the BGCs in cold seep sediments. Overall, these results demonstrate cold seep sediments potentially serve as a reservoir of hidden natural products and provide insights into microbial adaptation in chemosynthetically-driven ecosystems.

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“…Cold seeps, which are widely distributed on the seafloor of the world’s oceans, play a crucial role in the global marine geochemical cycling of carbon and sulfur [ 1 , 2 , 3 ]. Cold seep environments are characterized by methane-rich fluid emissions and distinctive sulfur oxidation–reduction reactions and support seabed oasis ecosystems composed of various kinds of high-productive microbial and faunal assemblages [ 2 , 4 , 5 , 6 , 7 ]. Therefore, diverse and abundant organic matter exists in cold seep environments, including gaseous and liquid hydrocarbons, aromatic compounds, polysaccharides, and biomass from chemosynthetic microorganisms and invertebrates [ 3 , 8 , 9 , 10 , 11 , 12 ].…”

Section: Introductionmentioning

confidence: 99%

The Phylogeny, Metabolic Potentials, and Environmental Adaptation of an Anaerobe, Abyssisolibacter sp. M8S5, Isolated from Cold Seep Sediments of the South China Sea

Liu,

Chen,

Wang

et al. 2023

Microorganisms

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Bacillota are widely distributed in various environments, owing to their versatile metabolic capabilities and remarkable adaptation strategies. Recent studies reported that Bacillota species were highly enriched in cold seep sediments, but their metabolic capabilities, ecological functions, and adaption mechanisms in the cold seep habitats remained obscure. In this study, we conducted a systematic analysis of the complete genome of a novel Bacillota bacterium strain M8S5, which we isolated from cold seep sediments of the South China Sea at a depth of 1151 m. Phylogenetically, strain M8S5 was affiliated with the genus Abyssisolibacter within the phylum Bacillota. Metabolically, M8S5 is predicted to utilize various carbon and nitrogen sources, including chitin, cellulose, peptide/oligopeptide, amino acids, ethanolamine, and spermidine/putrescine. The pathways of histidine and proline biosynthesis were largely incomplete in strain M8S5, implying that its survival strictly depends on histidine- and proline-related organic matter enriched in the cold seep ecosystems. On the other hand, strain M8S5 contained the genes encoding a variety of extracellular peptidases, e.g., the S8, S11, and C25 families, suggesting its capabilities for extracellular protein degradation. Moreover, we identified a series of anaerobic respiratory genes, such as glycine reductase genes, in strain M8S5, which may allow it to survive in the anaerobic sediments of cold seep environments. Many genes associated with osmoprotectants (e.g., glycine betaine, proline, and trehalose), transporters, molecular chaperones, and reactive oxygen species-scavenging proteins as well as spore formation may contribute to its high-pressure and low-temperature adaptations. These findings regarding the versatile metabolic potentials and multiple adaptation strategies of strain M8S5 will expand our understanding of the Bacillota species in cold seep sediments and their potential roles in the biogeochemical cycling of deep marine ecosystems.

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Unexpected genetic and microbial diversity for arsenic cycling in deep sea cold seep sediments

Cited by 5 publications

References 78 publications

Phylogenetically and structurally diverse reductive dehalogenases link biogeochemical cycles in deep-sea cold seeps

Phylogenetically and structurally diverse reductive dehalogenases link biogeochemical cycles in deep-sea cold seeps

A vast repertoire of secondary metabolites influences community dynamics and biogeochemical processes in cold seeps

The Phylogeny, Metabolic Potentials, and Environmental Adaptation of an Anaerobe, Abyssisolibacter sp. M8S5, Isolated from Cold Seep Sediments of the South China Sea

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