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One step beyond a ribosome: The ancient anaerobic core

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Sousa, Filipa L., Nelson-Sathi, Shijulal, Martin, William F.·2016·Biochimica et Biophysica Acta (BBA) - Bioenergetics
DOI 10.1016/j.bbabio.2016.04.284PMC PMC4906156
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Abstract

Life arose in a world without oxygen and the first organisms were anaerobes. Here we investigate the gene repertoire of the prokaryote common ancestor, estimating which genes it contained and to which lineages of modern prokaryotes it was most similar in terms of gene content. Using a phylogenetic approach we found that among trees for all 8779 protein families shared between 134 archaea and 1847 bacterial genomes, only 1045 have sequences from at least two bacterial and two archaeal groups and retain the ancestral archaeal-bacterial split. Among those, the genes shared by anaerobes were identified as candidate genes for the prokaryote common ancestor, which lived in anaerobic environments. We find that these anaerobic prokaryote common ancestor genes are today most frequently distributed among methanogens and clostridia, strict anaerobes that live from low free energy changes near the thermodynamic limit of life. The anaerobic families encompass genes for bifunctional acetyl-CoA-synthase/CO-dehydrogenase, heterodisulfide reductase subunits C and A, ferredoxins, and several subunits of the Mrp-antiporter/hydrogenase family, in addition to numerous S-adenosyl methionine (SAM) dependent methyltransferases. The data indicate a major role for methyl groups in the metabolism of the prokaryote common ancestor. The data furthermore indicate that the prokaryote ancestor possessed a rotor stator ATP synthase, but lacked cytochromes and quinones as well as identifiable redox-dependent ion pumping complexes. The prokaryote ancestor did possess, however, an Mrp-type H(+)/Na(+) antiporter complex, capable of transducing geochemical pH gradients into biologically more stable Na(+)-gradients. The findings implicate a hydrothermal, autotrophic, and methyl-dependent origin of life. This article is part of a Special Issue entitled 'EBEC 2016: 19th European Bioenergetics Conference, Riva del Garda, Italy, July 2-6, 2016', edited by Prof. Paolo Bernardi.

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  • The fact that the peptidyl transferase at the center of modern ribosomes is still a ribozyme provides support for an early role of RNA catalysis.

    “The fact that the peptidyl transferase at the center of modern ribosomes is still a ribozyme provides support for an early role of RNA catalysis [119,120,121].”

    From Opinion: The Key Steps in the Origin of Life to the Formation of the Eukaryotic Cell (2024) · cites this paper as [121]

    The Results and discussion section (‘Universal (or nearly so) genes’; page unavailable) says the protein sets indicate ribosomes were present in LUCA. It does not address whether modern peptidyl transferase is a ribozyme or whether that supports early RNA catalysis. Searches for peptidyl transferase, RNA catalysis, and ribozyme found no passage making that point. (LLM, conf=0.72)

    Experimental — accuracy not yet measured

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Authors
Sousa, F. L., Nelson-Sathi, S., & Martin, W. F.
Affiliations
Heinrich Heine University Düsseldorf (DE)
Corresponding author
Sousa, Filipa L.
ORCID
Venue
Biochimica et Biophysica Acta (BBA) - Bioenergetics
Publisher
Elsevier BV
Published
2016-08
Volume
1857
Issue
8
Pages
1027-1038
ISSN
0005-2728 (ISSN-L)
DOI
10.1016/j.bbabio.2016.04.284
PMC
PMC4906156
OpenAlex
W2346113366
Cited by
58
References
124
Citations by year
2026: 2 · 2025: 2 · 2024: 8 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 6 · 2019: 9 · 2018: 3 · 2017: 6 · 2016: 5
FWCI
3.67
Type
journal article
Language
en
Open access
Licence
Locations
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
ERC (666053)
Topics
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords
gene repertoire, methanogenic archaea, Clostridia, methyltransferase, heterodisulfide reductase, ferredoxin, hydrogenase, origin of life
MeSH terms
Clostridiales, Eubacteriales, Origin of Life, Anaerobiosis, Archaea, Bacterial Proteins, Coenzyme A Ligases, Biological Evolution, Ferredoxins, Hydrogenase, Methyltransferases, Phylogeny, Ribosomes, Protein Biosynthesis, Methanobacteriaceae, Archaeal Proteins, Metabolic Networks and Pathways, Molecular Sequence Annotation

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