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Cited by 32Microbial Community Ecology and PhysiologyOrigins and Evolution of LifeMethane Hydrates and Related Phenomena

Unique H2-utilizing lithotrophy in serpentinite-hosted systems

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Nobu, Masaru Konishi, Nakai, Ryosuke, Tamazawa, Satoshi, Mori, Hiroshi, Toyoda, Atsushi, Ijiri, Akira, Suzuki, Shino, Kurokawa, Ken +2 more·2023·The ISME Journal
DOI 10.1038/s41396-022-01197-9PMC PMC9751293
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Abstract

Serpentinization of ultramafic rocks provides molecular hydrogen (H2) that can support lithotrophic metabolism of microorganisms, but also poses extremely challenging conditions, including hyperalkalinity and limited electron acceptor availability. Investigation of two serpentinization-active systems reveals that conventional H2-/CO2-dependent homoacetogenesis is thermodynamically unfavorable in situ due to picomolar CO2 levels. Through metagenomics and thermodynamics, we discover unique taxa capable of metabolism adapted to the habitat. This included a novel deep-branching phylum, “Ca. Lithacetigenota”, that exclusively inhabits serpentinite-hosted systems and harbors genes encoding alternative modes of H2-utilizing lithotrophy. Rather than CO2, these putative metabolisms utilize reduced carbon compounds detected in situ presumably serpentinization-derived: formate and glycine. The former employs a partial homoacetogenesis pathway and the latter a distinct pathway mediated by a rare selenoprotein—the glycine reductase. A survey of microbiomes shows that glycine reductases are diverse and nearly ubiquitous in serpentinite-hosted environments. “Ca. Lithacetigenota” glycine reductases represent a basal lineage, suggesting that catabolic glycine reduction is an ancient bacterial innovation by Terrabacteria for gaining energy from geogenic H2 even under hyperalkaline, CO2-poor conditions. Unique non-CO2-reducing metabolisms presented here shed light on potential strategies that extremophiles may employ for overcoming a crucial obstacle in serpentinization-associated environments, features potentially relevant to primordial lithotrophy in early Earth.

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  • No archaea were detected in Hakuba Happo, but glycine reductase utilizing Lithacetigenota were detected at the Cedars.

    “No archaea were detected in Hakuba Happo, but glycine reductase utilizing Lithacetigenota were detected at the Cedars (Nobu et al., 2023).”

    From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Nobu et al., 2023

    The Thermodynamics and geochemistry section says archaea were absent in Hakuba, and the Diverse putative H2- and formate-utilizing organisms section reports “Ca. Lithacetigenota” at The Cedars. The site-adapted metabolism section reports glycine reductases in The Cedars population but says it *may* perform glycine reduction; it does not establish actual utilization. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • The findings of Nobu et al. (2023) suggest that geochemical nitrogen fixation to amino acids is ongoing today, continuously in the hyperalkaline serpentinizing environment of Hakuba Happo.

    “The findings of Nobu et al. (2023) suggest that it is ongoing today, continuously in the hyperalkaline serpentinizing environment of Hakuba Happo.”

    From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Nobu et al., 2023

    In the “Ca. Lithacetigenota” section (page unavailable), the paper reports glycine in Hakuba water and suspects that some is generated geochemically in situ. That supports a suggestion of present-day amino-acid formation, but the paper does not establish that it occurs continuously. Its proposed route uses NH3 to form glycine; it does not show geochemical fixation of nitrogen to amino acids. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Nobu et al. (2023) recently reported the presence of glycine (5 nM) in the effluent of Hakuba Happo which is likely of abiotic origin.

    “Nobu et al. (2023) recently reported the presence of glycine (5 nM) in the effluent of Hakuba Happo which is likely of abiotic origin.”

    From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Nobu et al., 2023

  • Available data indicate that the crust can generate reduced nitrogen in serpentinizing systems and phosphite during serpentinization, with carbon and sulfur reduction reactions being facile under serpentinizing conditions.

    “Available data indicate that the crust can generate reduced nitrogen in serpentinizing systems (Nobu et al., 2023; Shang et al., 2023b) and phosphite during serpentinization (Pasek et al., 2022), with carbon and sulfur reduction reactions being facile under serpentinizing conditions.”

    From Serpentinization as the source of energy, electrons, organics, catalysts, nutrients and pH gradients for the origin of LUCA and life (2023) · cites this paper as Nobu et al., 2023

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Cited by

Sorted by citations

Authors
Nobu, M. K., Nakai, R., Tamazawa, S., Mori, H., Toyoda, A., Ijiri, A., Suzuki, S., Kurokawa, K., Kamagata, Y., & Tamaki, H.
Affiliations
  • National Institute of Advanced Industrial Science and Technology (JP)
  • Biomanufacturing Process Research Center (JP)
  • North Advancement Center for Science and Technology (JP)
  • National Institute of Genetics (JP)
  • Japan Agency for Marine-Earth Science and Technology (JP)
Corresponding author
  • Nobu, Masaru Konishi
  • Tamaki, Hideyuki
ORCID
Venue
The ISME Journal
Publisher
Oxford University Press (OUP)
Published
2022-10-07
Volume
17
Issue
1
Pages
95-104
ISSN
  • 1751-7362 (ISSN-L)
  • 1751-7370
DOI
10.1038/s41396-022-01197-9
PMC
PMC9751293
OpenAlex
W4303446484
Cited by
32
References
15
Citations by year
2026: 7 · 2025: 6 · 2024: 9 · 2023: 9 · 2022: 1
FWCI
3.33
Type
journal article
Language
en
Open access
Licence
Locations
  • The ISME Journal (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
MEXT | Japan Society for the Promotion of Science (JP26710012, JP18H02426, JP18H03367, JP15H05620, JP26106006, JP26106004)
Topics
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Physical Sciences › Environmental Science › Environmental Chemistry › Methane Hydrates and Related Phenomena
Keywords
serpentinization, homoacetogenesis, glycine reductase, selenoproteins, formate metabolism, glycine metabolism, extremophiles, ultramafic rocks, microbial metabolism
MeSH terms
Glycine, Hydrogen, Oxidoreductases, Magnesium Silicates, Autotrophic Processes, Microbiota

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