Deep microbial proliferation at the basalt interface in 33.5–104 million-year-old oceanic crust

Suzuki, Yohey; Yamashita, Seiya; Kouduka, Mariko; Ao, Yutaro; Mukai, Hiroki; Mitsunobu, Satoshi; Kagi, Hiroyuki; Dhondt, Steven; Inagaki, Fumio; Morono, Yuki; Hoshino, Takao; Tomioka, Naotaka; Ito, Motoo

doi:10.1038/s42003-020-0860-1

Cited by 41 publications

(49 citation statements)

References 47 publications

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“…The greenish cell-like signals from the DNA dye and the overlapped NanoSIMS mapping of P and CN are consistent with results from previous study of microbial cells in mineral-filled cracks 9 . However, the appearance of individual cells was not clear, in contrast to the earlier work.…”

Section: Resultssupporting

confidence: 91%

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Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

Takamiya

Kouduka

Furutani

et al. 2021

Preprint

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Chemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. In contrast to actively venting chimneys, the nature of microbial life in extinct chimneys without fluid venting remains largely unknown. Here, the occurrence of ultra-small cells in silica-filled grain boundaries inside an extinct chimney is demonstrated by high-resolution bio-signature mapping. The ultra-small cells are associated with extracellularly precipitated Cu2O nanocrystals. Single-gene analysis shows that the chimney interior is dominated by a member of Pacearchaeota known as a major phylum of DPANN. Genome-resolved metagenomic analysis reveals that the chimney Pacearchaeota member is equipped with a nearly full set of genes for fermentation-based energy generation from nucleic acids, in contrast to previously characterized Pacearchaeota members lacking many genes for nucleic acid fermentation. We infer that the ultra-small cells associated with silica and extracellular Cu2O nanocrystals in the grain boundaries are Pacearchaeota, on the basis of the experimentally demonstrated capability of silica to concentrate nucleic acids from seawater and the presence of Cu-exporting genes in a reconstructed Pacearchaeota genome. Given the existence of ~3-billion-year-old submarine hydrothermally deposited silica, proliferation of microbial life using silica-bound nucleic acids might be relevant to the primitive vent biosphere.

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Section: Resultssupporting

confidence: 91%

“…Analytical procedures have been developed to visualize and quantify microbial cells hosted in crack-infilling minerals in the oceanic crust by preparing thin sections of rocks embedded in hydrophilic resin called LR White 8,9 . Microbial cells embedded in the resin are stainable with a DNA dye called SYBR-Green I.…”

Section: Resultsmentioning

confidence: 99%

Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

Takamiya

Kouduka

Furutani

et al. 2021

Preprint

Self Cite

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“…Chemosynthetic DOC produced in situ is likely turned over rapidly in the shallow crustal fluids, but Δ 14 C values in the Deep horizon of U1383C suggest a net contribution of 14 C-enriched DOC from chemoautotrophy [10]. Two recent microbial studies of subseafloor rocks recovered via ocean drilling showed a dominance of heterotrophic bacteria and little evidence for autotrophic processes [57,58].…”

Section: Carbon Fixation and Turnovermentioning

confidence: 99%

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

et al. 2020

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The oceanic crustal aquifer is one of the largest habitable volumes on Earth, and it harbors a reservoir of microbial life that influences global-scale biogeochemical cycles. Here, we use time series metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. We also present metagenome-assembled genomes from recently collected fluids that are furthest removed from drilling disturbances. Our results suggest that the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust. This community is motile and metabolically flexible, with the ability to use both autotrophic and organotrophic pathways, as well as function under low oxygen conditions by using alternative electron acceptors such as nitrate and thiosulfate. Anaerobic processes are most abundant in subseafloor horizons deepest in the aquifer, furthest from connectivity with the deep ocean, and there was little overlap in the active microbial populations between sampling horizons. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.

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“…However, these experiments also showed evidence for biomass production from DIC, and rates of activity varied over 8 orders of magnitude for both inorganic and organic carbon uptake, consistent with the mixotrophic genetic signatures observed in our study. Two recent microbial studies of subseafloor rocks recovered via ocean drilling also showed a dominance of heterotrophic bacteria and little evidence for autotrophic processes [58,59], suggesting mixotrophy and heterotrophy may be a common strategy in the cool, crustal subseafloor habitat.…”

Section: Carbon Fixation and Turnovermentioning

confidence: 99%

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

Seyler

Trembath‐Reichert

Tully

et al. 2020

Preprint

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The rock-hosted oceanic crustal aquifer is one of the largest habitable volumes on Earth, and it harbors a reservoir of microbial life that influences global-scale biogeochemical cycles. Here, we use time series metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment that is representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. The data suggest that the microbial community in this subseafloor habitat is motile, chiefly heterotrophic or mixotrophic, and capable of using alternative electron acceptors such as nitrate and thiosulfate, in addition to oxygen. Anaerobic processes are most abundant in subseafloor horizons deepest in the aquifer, furthest from connectivity with the deep ocean, and there was little overlap in the active microbial populations between sampling horizons. Together, our results indicate the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust, and is also metabolically flexible, with the ability to switch from autotrophy to heterotrophy, as well as function under low oxygen conditions. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.

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Deep microbial proliferation at the basalt interface in 33.5–104 million-year-old oceanic crust

Cited by 41 publications

References 47 publications

Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

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