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Title: Remnants of an Ancient Metabolism without Phosphate

Abstract

Phosphate is essential for all living systems, serving as a building block of genetic and metabolic machinery. However, it is unclear how phosphate could have assumed these central roles on primordial Earth, given its poor geochemical accessibility. We used systems biology approaches to explore the alternative hypothesis that a protometabolism could have emerged prior to the incorporation of phosphate. Surprisingly, we identified a cryptic phosphate-independent core metabolism producible from simple prebiotic compounds. This network is predicted to support the biosynthesis of a broad category of key biomolecules. Its enrichment for enzymes utilizing iron-sulfur clusters, and the fact that thermodynamic bottlenecks are more readily overcome by thioester rather than phosphate couplings, suggest that this network may constitute a ‘‘metabolic fossil’’ of an early phosphate-free nonenzymatic biochemistry. Thus, our results corroborate and expand previous proposals that a putative thioester-based metabolism could have predated the incorporation of phosphate and an RNA-based genetic system.

Authors:
 [1];  [2];  [3];  [4]
  1. Boston Univ., MA (United States). Bioinformatics Program
  2. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Earth, Atmosphere and Planetary Science Dept.
  3. Boston Univ., MA (United States). Bioinformatics Program and Dept. of Biomedical Engineering
  4. Boston Univ., MA (United States). Bioinformatics Program and Dept. of Biomedical Engineering and Dept. of Biology and Dept. of Physics
Publication Date:
Research Org.:
Boston Univ., MA (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF); European Union (EU); National Institutes of Health (NIH)
OSTI Identifier:
1377637
Alternate Identifier(s):
OSTI ID: 1425650
Grant/Contract Number:
SC0012627; DEB-07NA273441457695; NSFOCE-BSF-1635070; T32GM100842
Resource Type:
Journal Article: Published Article
Journal Name:
Cell
Additional Journal Information:
Journal Volume: 168; Journal Issue: 6; Journal ID: ISSN 0092-8674
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; origin of life; phosphate; thioester world; network expansion; systems biology

Citation Formats

Goldford, Joshua E., Hartman, Hyman, Smith, Temple F., and Segrè, Daniel. Remnants of an Ancient Metabolism without Phosphate. United States: N. p., 2017. Web. doi:10.1016/j.cell.2017.02.001.
Goldford, Joshua E., Hartman, Hyman, Smith, Temple F., & Segrè, Daniel. Remnants of an Ancient Metabolism without Phosphate. United States. doi:10.1016/j.cell.2017.02.001.
Goldford, Joshua E., Hartman, Hyman, Smith, Temple F., and Segrè, Daniel. Thu . "Remnants of an Ancient Metabolism without Phosphate". United States. doi:10.1016/j.cell.2017.02.001.
@article{osti_1377637,
title = {Remnants of an Ancient Metabolism without Phosphate},
author = {Goldford, Joshua E. and Hartman, Hyman and Smith, Temple F. and Segrè, Daniel},
abstractNote = {Phosphate is essential for all living systems, serving as a building block of genetic and metabolic machinery. However, it is unclear how phosphate could have assumed these central roles on primordial Earth, given its poor geochemical accessibility. We used systems biology approaches to explore the alternative hypothesis that a protometabolism could have emerged prior to the incorporation of phosphate. Surprisingly, we identified a cryptic phosphate-independent core metabolism producible from simple prebiotic compounds. This network is predicted to support the biosynthesis of a broad category of key biomolecules. Its enrichment for enzymes utilizing iron-sulfur clusters, and the fact that thermodynamic bottlenecks are more readily overcome by thioester rather than phosphate couplings, suggest that this network may constitute a ‘‘metabolic fossil’’ of an early phosphate-free nonenzymatic biochemistry. Thus, our results corroborate and expand previous proposals that a putative thioester-based metabolism could have predated the incorporation of phosphate and an RNA-based genetic system.},
doi = {10.1016/j.cell.2017.02.001},
journal = {Cell},
number = 6,
volume = 168,
place = {United States},
year = {Thu Mar 09 00:00:00 EST 2017},
month = {Thu Mar 09 00:00:00 EST 2017}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1016/j.cell.2017.02.001

Citation Metrics:
Cited by: 12works
Citation information provided by
Web of Science

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  • Phosphate is essential for all living systems, serving as a building block of genetic and metabolic machinery. However, it is unclear how phosphate could have assumed these central roles on primordial Earth, given its poor geochemical accessibility. We used systems biology approaches to explore the alternative hypothesis that a protometabolism could have emerged prior to the incorporation of phosphate. Surprisingly, we identified a cryptic phosphate-independent core metabolism producible from simple prebiotic compounds. This network is predicted to support the biosynthesis of a broad category of key biomolecules. Its enrichment for enzymes utilizing iron-sulfur clusters, and the fact that thermodynamic bottlenecksmore » are more readily overcome by thioester rather than phosphate couplings, suggest that this network may constitute a ‘‘metabolic fossil’’ of an early phosphate-free nonenzymatic biochemistry. Thus, our results corroborate and expand previous proposals that a putative thioester-based metabolism could have predated the incorporation of phosphate and an RNA-based genetic system.« less
  • No abstract prepared.
  • We report crystal structures of the citrate and sn-glycerol-1-phosphate (G1P) complexes of (S)-3-O-geranylgeranylglyceryl phosphate synthase from Archaeoglobus fulgidus (AfGGGPS) at 1.55 and 2.0 {angstrom} resolution, respectively. AfGGGPS is an enzyme that performs the committed step in archaeal lipid biosynthesis, and it presents the first triose phosphate isomerase (TIM)-barrel structure with a prenyltransferase function. Our studies provide insight into the catalytic mechanism of AfGGGPS and demonstrate how it selects for the sn-G1P isomer. The replacement of 'Helix 3' by a 'strand' in AfGGGPS, a novel modification to the canonical TIM-barrel fold, suggests a model of enzyme adaptation that involves a 'greasymore » slide' and a 'swinging door.' We propose functions for the homologous PcrB proteins, which are conserved in a subset of pathogenic bacteria, as either prenyltransferases or being involved in lipoteichoic acid biosynthesis. Sequence and structural comparisons lead us to postulate an early evolutionary history for AfGGGPS, which may highlight its role in the emergence of Archaea.« less
  • The pathway construction for biosynthesis of aromatic amino acids in Escherichia coli is atypical of the phylogenetic subdivision of gram-negative bacteria to which it belongs. Related organisms possess second pathways to phenylalanine and tyrosine which depend upon the expression of a monofunctional chorismate mutase (CM-F) and cyclohexadienyl dehydratase (CDT). Some enteric bacteria, unlike E. coli, possess either CM-F or CDT. These essentially cryptic remnants of an ancestral pathway can be a latent source of biochemical potential under certain conditions. As one example of advantageous biochemical potential, the presence of CM-F in Salmonella typhimurium increases the capacity for prephenate accumulation inmore » a tyrA auxotroph. We report the finding that a significant fraction of the latter prephenate is transaminated to L-arogenate. The tyrA19 mutant is now the organism of choice for isolation of L-arogenate, uncomplicated by the presence of other cyclohexadienyl products coaccumulated by a Neurospora crassa mutant that had previously served as the prime biological source of L-arogenate. Prephenate aminotransferase activity was not conferred by a discrete enzyme, but rather was found to be synonymous with the combined activities of aspartate aminotransferase (aspC), aromatic aminotransferase (tyrB), and branched-chain aminotransferase (ilvE).« less