Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons

Abstract

In ambiguous stop/sense genetic codes, the stop codon(s) not only terminate translation but can also encode amino acids. Such codes have evolved at least four times in eukaryotes, twice among ciliates (Condylostoma magnum and Parduczia sp.). These have appeared to be isolated cases whose next closest relatives use conventional stop codons. However, little genomic data have been published for the Karyorelictea, the ciliate class that contains Parduczia sp., and previous studies may have overlooked ambiguous codes because of their apparent rarity. We therefore analyzed single-cell transcriptomes from four of the six karyorelict families to determine their genetic codes. Reassignment of canonical stops to sense codons was inferred from codon frequencies in conserved protein domains, while the actual stop codon was predicted from full-length transcripts with intact 3'-UTRs. We found that all available karyorelicts use the Parduczia code, where canonical stops UAA and UAG are reassigned to glutamine, and UGA encodes either tryptophan or stop. Furthermore, a small minority of transcripts may use an ambiguous stop-UAA instead of stop-UGA. Given the ubiquity of karyorelicts in marine coastal sediments, ambiguous genetic codes are not mere marginal curiosities but a defining feature of a globally distributed and abundant group of eukaryotes.

Nuclear dualism without extensive DNA elimination in the ciliateLoxodes magnus

“…Karyorelicts including Loxodes generally use an ambiguous stop/sense genetic code (NCBI translation table 27) where the only stop codon, UGA, can also encode tryptophan (W) if sufficiently far upstream of the mRNA poly(A) tail. 45,46 Coding UGAs must be distinguished from stop UGAs to predict genes, but existing software does not permit single codons with alternative, context-dependent translation outcomes.…”