A digital DNA system reveals the superiority of unidirectional inheritance over 'Lamarckian' inheritance

Abstract

In biology, changes to a DNA sequence can impact protein sequence but changes to protein sequence (phenotype) do not flow back into DNA (genotype). A system with bidirectional information flow (i.e. both translation and 'reverse translation') remains a theoretical possibility for an independent origin of life or an artificial biosystem, but the recent development of digital data storage in DNA does just this: changes made to a digital file can be written back into DNA, meaning changes to 'phenotype' can be written back to 'genotype'. To explore the evolutionary properties of such a system, we created an artificial system where synthetic DNA serves as genotype and music as phenotype. Audio can be output from a DNA sequence, then recorded and written to DNA as 'codons', enabling bidirectional information flow (DNA→music and music→DNA). Our results show that the mutation rate in a bidirectional system is much higher than for unidirectional information flow, and that, under reverse translation there is no mechanism for preservation of codon choice across generations. This has the effect of eliminating the impact of spontaneous synonymous mutations, a key the benefit of a redundant genetic code. As a result, non-synonymous mutations are the only DNA-level changes that are transmitted across generations, and, as non-synonymous mutation can emerge at both 'genotypic' and 'phenotypic' levels, these occur at a two-fold higher frequency than in a unidirectional system. Our system holds some practical insight. First, for DNA read/write systems, it may be wise to avoid designing systems with 'de novo reverse translation' because the opportunities for mutation are higher; tracking genotype information from the preceding generation to guide this process may reduce error. Second, our system helps clarify how a 'Lamarckian' biological system might operate. We conclude that, were a 'Lamarckian' system of inheritance a feature of early genetic systems, it would likely have been short lived as the high frequency of mutation would risk driving the system to extinction. A system based on unidirectional information flow thus appears superior as there are fewer opportunities for mutational error.

Competing Interest Statement

The authors have declared no competing interest.