Abstract
We study the potential for the de novo evolution of genes from random nucleotide sequences using libraries of E. coli expressing random sequence peptides. We assess the effects of such peptides on cell growth by monitoring frequency changes in individual clones in a complex library through four serial passages. Using a new analysis pipeline that allows the tracing of peptides of all lengths, we find that over half of the peptides have consistent effects on cell growth. Across nine different experiments, around 16% of clones increase in frequency and 36% decrease, with some variation between individual experiments. Shorter peptides (8–20 residues), are more likely to increase in frequency, longer ones are more likely to decrease. GC content, amino acid composition, intrinsic disorder, and aggregation propensity show slightly different patterns between peptide groups. Sequences that increase in frequency tend to be more disordered with lower aggregation propensity. This coincides with the observation that young genes with more disordered structures are better tolerated in genomes. Our data indicate that random sequences can be a source of evolutionary innovation, since a large fraction of them are well tolerated by the cells or can provide a growth advantage.
Highlights
New genes can arise by two alternative mechanisms [1,2,3,4,5,6]
We study the potential for the de novo evolution of genes from random nucleotide sequences using libraries of E. coli expressing random sequence peptides
No single determining feature of a sequence could be identified that would earmark individual peptides as having potentially positive or negative effects on the cells, some differences exist with respect to structural properties
Summary
New genes can arise by two alternative mechanisms [1,2,3,4,5,6]. The first is through duplication and/or recombination of existing genes or gene fragments, which later accumulate mutations that render them different from their parental genes. Overall genome comparisons between recently separated species have suggested that de novo evolved genes arise continuously with a high rate, but can get lost at high rates [25,26,27,28]. This dynamic transformation of non-coding sequences into coding ones is very clear, especially in eukaryotes, where large parts of the non-coding genome are transcribed. Comparisons between closely related mouse populations and species revealed the transcription of these non-coding regions is subject to fast evolutionary change, such that within a time span of 10 million years the whole genome can become transcribed and subjected to evolutionary testing [8]. The raw material for de novo evolution, namely transcripts from initially non-coding DNA regions, is abundantly present
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