Tracing the evolution of the plastome and mitogenome in the chloropicophyceae uncovered convergent tRNA gene losses and a variant plastid genetic code

Abstract

The tiny green algae belonging to the Chloropicophyceae play a key role inmarine phytoplankton communities; this newly erected class of prasinophytes comprises two genera (Chloropicon and Chloroparvula) containing each several species.We sequenced the plastomes and mitogenomes of eight Chloropicon and five Chloroparvula species to better delineate the phylogenetic affinities of these taxa and to infer the suite of changes that their organelle genomes sustained during evolution. The relationships resolved in organelle-based phylogenomic treeswere essentially congruentwith previously reported rRNAtrees, and similar evolutionary trends but distinct dynamicswere identified for the plastome and mitogenome. Although the plastome sustained considerable changes in gene content and order at the time the two genera split, subsequently it remained stable and maintained a very small size. The mitogenome, however, was remodeled more gradually and showed more fluctuation in size, mainly as a result of expansions/contractions of intergenic regions. Remarkably, the plastome and mitogenome lost a common set of three tRNA genes, with the trnI(cau) andtrnL(uaa) lossesbeingaccompaniedwithimportant variations in codonusage.Unexpectedly,despite the disappearance of trnI(cau) fromthe plastomein theChloroparvula lineage,AUAcodons (the codons recognizedby thisgeneproduct)were detected in certain plastid genes. By comparing the sequences of plastid protein-coding genes fromchloropicophycean and phylogenetically diverse chlorophyte algae with those of the corresponding predicted proteins, we discovered that the AUA codon was reassigned from isoleucine to methionine in Chloroparvula. This noncanonical genetic code has not previously been uncovered in plastids.