Abstract:
BACKGROUND:There is wide agreement that only a subset of the twenty standard amino acids existed prebiotically in sufficient concentrations to form functional polypeptides. We ask how this subset, postulated as {A,D,E,G,I,L,P,S,T,V}, could have formed structures stable enough to found metabolic pathways. Inspired by alphabet reduction experiments, we undertook a computational analysis to measure the structural coding behavior of sequences simplified by reduced alphabets. We sought to discern characteristics of the prebiotic set that would endow it with unique properties relevant to structure, stability, and folding. RESULTS:Drawing on a large dataset of single-domain proteins, we employed an information-theoretic measure to assess how well the prebiotic amino acid set preserves fold information against all other possible ten-amino acid sets. An extensive virtual mutagenesis procedure revealed that the prebiotic set excellently preserves sequence-dependent information regarding both backbone conformation and tertiary contact matrix of proteins. We observed that information retention is fold-class dependent: the prebiotic set sufficiently encodes the structure space of α/β and α + β folds, and to a lesser extent, of all-α and all-β folds. The prebiotic set appeared insufficient to encode the small proteins. Assessing how well the prebiotic set discriminates native vs. incorrect sequence-structure matches, we found that α/β and α + β folds exhibit more pronounced energy gaps with the prebiotic set than with nearly all alternatives. CONCLUSIONS:The prebiotic set optimally encodes local backbone structures that appear in the folded environment and near-optimally encodes the tertiary contact matrix of extant proteins. The fold-class-specific patterns observed from our structural analysis confirm the postulated timeline of fold appearance in proteogenesis derived from proteomic sequence analyses. Polypeptides arising in a prebiotic environment will likely form α/β and α + β-like folds if any at all. We infer that the progressive expansion of the alphabet allowed the increased conformational stability and functional specificity of later folds, including all-α, all-β, and small proteins. Our results suggest that prebiotic sequences are amenable to mutations that significantly lower native conformational energies and increase discrimination amidst incorrect folds. This property may have assisted the genesis of functional proto-enzymes prior to the expansion of the full amino acid alphabet.
journal_name
BMC Evol Bioljournal_title
BMC evolutionary biologyauthors
Solis ADdoi
10.1186/s12862-019-1464-6subject
Has Abstractpub_date
2019-07-30 00:00:00pages
158issue
1issn
1471-2148pii
10.1186/s12862-019-1464-6journal_volume
19pub_type
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