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Cited by 101Microbial metabolism and enzyme functionOrigins and Evolution of LifeAnaerobic Digestion and Biogas Production

Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism

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Sousa, Filipa L., Martin, William F.·2014·Biochimica et Biophysica Acta (BBA) - Bioenergetics
DOI 10.1016/j.bbabio.2014.02.001
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Abstract

The deep dichotomy of archaea and bacteria is evident in many basic traits including ribosomal protein composition, membrane lipid synthesis, cell wall constituents, and flagellar composition. Here we explore that deep dichotomy further by examining the distribution of genes for the synthesis of the central carriers of one carbon units, tetrahydrofolate (H4F) and tetrahydromethanopterin (H4MPT), in bacteria and archaea. The enzymes underlying those distinct biosynthetic routes are broadly unrelated across the bacterial-archaeal divide, indicating that the corresponding pathways arose independently. That deep divergence in one carbon metabolism is mirrored in the structurally unrelated enzymes and different organic cofactors that methanogens (archaea) and acetogens (bacteria) use to perform methyl synthesis in their H4F- and H4MPT-dependent versions, respectively, of the acetyl-CoA pathway. By contrast, acetyl synthesis in the acetyl-CoA pathway - from a methyl group, CO2 and reduced ferredoxin - is simpler, uniform and conserved across acetogens and methanogens, and involves only transition metals as catalysts. The data suggest that the acetyl-CoA pathway, while being the most ancient of known CO2 assimilation pathways, reflects two phases in early evolution: an ancient phase in a geochemically confined and non-free-living universal common ancestor, in which acetyl thioester synthesis proceeded spontaneously with the help of geochemically supplied methyl groups, and a later phase that reflects the primordial divergence of the bacterial and archaeal stem groups, which independently invented genetically-encoded means to synthesize methyl groups via enzymatic reactions. This article is part of a Special Issue entitled: 18th European Bioenergetic Conference.

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Crossref · 10.1016/j.bbabio.2014.02.001

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  • Pterin-dependent methyl synthesis pathways likely arose independently post-LUCA in the lineages leading to bacteria and archaea.

    “while pterin‐dependent methyl synthesis pathways likely arose independently post‐LUCA in the lineages leading to bacteria and archaea.”

    From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [50]

  • The evidence for corrin antiquity stems from its essential role in the acetyl-CoA pathway, the most ancient among CO2-fixing pathways.

    “The evidence for corrin antiquity stems from its essential role in the acetyl‐CoA pathway, the most ancient among CO2‐fixing pathways [48, 49, 50, 51].”

    From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [50]

  • The common ancestor of acetogens and methanogens was dependent upon a supply of chemically reactive methyl groups provided by the environment.

    “This in turn suggests that the common ancestor of acetogens and methanogens was dependent upon a supply of chemically reactive methyl groups provided by the environment [47, 50]”

    From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [50]

  • Several other studies uncovered further examples in which individual genes of the archaeal methyl synthesis and methanopterin pathways had been transferred from archaea to bacterial recipients, which are often O2-dependent methylotrophs and methanotrophs.

    “Several other studies uncovered further examples in which individual genes of the archaeal methyl synthesis and methanopterin pathways had been transferred from archaea to bacterial recipients [50, 151, 152, 153, 154], which are often O2‐dependent methylotrophs and methanotrophs.”

    From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [50]

  • The presence of corrin synthesis in LUCA contrasts with the lack of homologous methyl synthesis branches across the bacterial and archaeal versions of the acetyl-CoA pathway that delivers methyl groups for CoFeS, suggesting that LUCA utilized geochemically supplied methyl groups.

    “The presence of corrin synthesis in LUCA contrasts with the lack of homologous methyl synthesis branches across the bacterial and archaeal versions of the acetyl‐CoA pathway that delivers methyl groups for CoFeS (Fig. 3), suggesting that LUCA utilized geochemically supplied methyl groups [47, 50].”

    From Evidence for corrin biosynthesis in the last universal common ancestor (2025) · cites this paper as [50]

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Authors
Sousa, F. L., & Martin, W. F.
Affiliations
Heinrich Heine University Düsseldorf (DE)
ORCID
Venue
Biochimica et Biophysica Acta (BBA) - Bioenergetics
Publisher
Elsevier BV
Published
2014-07
Volume
1837
Issue
7
Pages
964-981
ISSN
0005-2728 (ISSN-L)
DOI
10.1016/j.bbabio.2014.02.001
OpenAlex
W2091419808
Cited by
100
References
234
Citations by year
2026: 8 · 2025: 6 · 2024: 8 · 2023: 7 · 2022: 7 · 2021: 11 · 2020: 8 · 2019: 8 · 2018: 11 · 2017: 9 · 2016: 8 · 2015: 6 · 2014: 3
FWCI
3.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
Funders
European Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Physical Sciences › Engineering › Building and Construction › Anaerobic Digestion and Biogas Production
Keywords
one-carbon metabolism, tetrahydrofolate, tetrahydromethanopterin, acetyl-CoA pathway, methanogenic archaea, acetogenic bacteria, carbon assimilation, ferredoxin, transition metals, prokaryotic metabolism
MeSH terms
Acetyl Coenzyme A, Archaea, Bacteria, Carbon, Energy Metabolism, Environment, Fossils, Genes, Bacterial, Pterins, Tetrahydrofolates, Evolution, Molecular, Genes, Archaeal

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