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Cited by 46Origins and Evolution of LifeMetalloenzymes and iron-sulfur proteinsMicrobial metabolism and enzyme function

Bioenergetic constraints on the origin of autotrophic metabolism

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Boyd, Eric S., Amenabar, Maximiliano J., Poudel, Saroj, Templeton, Alexis S.·2020·Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
DOI 10.1098/rsta.2019.0151PMC PMC7015307
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Abstract

Autotrophs form the base of all complex food webs and seemingly have done so since early in Earth history. Phylogenetic evidence suggests that early autotrophs were anaerobic, used CO 2 as both an oxidant and carbon source, were dependent on H 2 as an electron donor, and used iron-sulfur proteins (termed ferredoxins) as a primary electron carrier. However, the reduction potential of H 2 is not typically low enough to efficiently reduce ferredoxin. Instead, in modern strictly anaerobic and H 2 -dependent autotrophs, ferredoxin reduction is accomplished using one of several recently evolved enzymatic mechanisms, including electron bifurcating and coupled ion translocating mechanisms. These observations raise the intriguing question of why anaerobic autotrophs adopted ferredoxins as central electron carriers only to have to evolve complex machinery to reduce them. Here, we report calculated reduction potentials for H 2 as a function of observed environmental H 2 concentration, pH and temperature. Results suggest that a combination of alkaline pH and high H 2 concentration yield H 2 reduction potentials low enough to efficiently reduce ferredoxins. Hyperalkaline, H 2 rich environments have existed in discrete locations throughout Earth history where ultramafic minerals are undergoing hydration through the process of serpentinization. These results suggest that serpentinizing systems, which would have been common on early Earth, naturally produced conditions conducive to the emergence of H 2 -dependent autotrophic life. The primitive process of hydrogenotrophic methanogenesis is used to examine potential changes in methanogenesis and Fd reduction pathways as these organisms diversified away from serpentinizing environments. This article is part of a discussion meeting issue ‘Serpentinite in the earth system’.

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  • The alkaline nature of effluent in serpentinizing systems, in the range of pH 9-11, stemming from continuous Mg(OH)2 synthesis during serpentinization, together with high H2 concentrations of 1-10 mM or more, generates extremely negative redox potentials, on the order of -435 to -830 mV.

    “First, the alkaline nature of effluent in serpentinizing systems, in the range of pH 9–11, stemming from continuous Mg (OH)2 synthesis during the serpentinization process (Chavagnac et al., 2013), together with high H2 concentrations of 1–10 mM or more, generates extremely negative redox potentials, on the order of –435 to –830 mV which where both measured and calculated at and for serpentinizing”

    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 Boyd et al., 2020

  • Because of the high alkalinity and high H2 concentration, the calculated redox potential of serpentinizing effluent can be in the range of -800 mV, sufficient for most biologically relevant reduction as shown in Figure 2, with the exception of the phosphate/phosphite couple.

    “Because of the high alkalinity and high H2 concentration, the calculated redox potential of serpentinizing effluent can be in the range of –800 mV (Boyd et al., 2020), sufficient for most biologically relevant reduction as shown in Figure 2, with the exception of the phosphate/phosphite couple, where the midpoint potentials become more negative with increasing pH (Bernhard Schink, pers. comm.).”

    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 Boyd et al., 2020

  • All of the essential reduction reactions underlying the conversion of the elements on the early Earth from their ancestrally oxidized states (CO2, N2, HPO42-, SO2) to their biologically relevant state - reduced C, NH3, H2S, and in the case of P, the biochemically accessible state - now appear to lie within the range that serpentinizing systems can generate naturally.

    “From that it follows that all of the essential reduction reactions underlying the conversion of the elements on the early Earth from their ancestrally oxidized states (CO2, N2, HPO42–, SO2) to their biologically relevant state — reduced C, NH3, H2S, and in the case of P, the biochemically accessible state — now appear to lie within the range that serpentinizing systems can generate naturally (Russ”

    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 Boyd et al., 2020

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Authors
Boyd, E. S., Amenabar, M. J., Poudel, S., & Templeton, A. S.
Affiliations
  • Montana State University (US)
  • Department of Microbiology and Immunology, Montana State University, Bozeman, MT 59717, USA
  • University of Colorado Boulder (US)
Corresponding author
Boyd, Eric S.
ORCID
Venue
Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences
Publisher
The Royal Society
Published
2020-01-06
Volume
378
Issue
2165
Pages
20190151
ISSN
  • 1364-503X (ISSN-L)
  • 1471-2962
DOI
10.1098/rsta.2019.0151
PMC
PMC7015307
OpenAlex
W2998604881
Cited by
46
References
54
Citations by year
2026: 2 · 2025: 5 · 2024: 8 · 2023: 8 · 2022: 5 · 2021: 10 · 2020: 8
FWCI
3.45
Type
journal article
Language
en
Open access
Licence
royalsociety.org/journals/ethics-policies/data-sharing-mining/ (tdm)
Locations
  • Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Aeronautics and Space Administration (NNA15BB02A)
  • Basic Energy Sciences (DE-SC0012518)
Topics
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Metalloenzymes and iron-sulfur proteins
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
Keywords
hydrogenotrophic methanogenesis, ferredoxin reduction, serpentinization, alkaline pH, early Earth, electron bifurcation, iron-sulfur proteins, bioenergetics
MeSH terms
Carbon, Carbon Dioxide, Energy Metabolism, Oxidation-Reduction, Temperature, Autotrophic Processes

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