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 in marine 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 trees were essentially congruent with previously reported rRNA trees, and similar evolutionary trends but distinct dynamics were 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) and trnL(uaa) losses being accompanied with important variations in codon usage. Unexpectedly, despite the disappearance of trnI(cau) from the plastome in the Chloroparvula lineage, AUA codons (the codons recognized by this gene product) were detected in certain plastid genes. By comparing the sequences of plastid protein-coding genes from chloropicophycean 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.

Mantoniella beaufortii and Mantoniella baffinensis sp. nov. (Mamiellales, Mamiellophyceae), two new green algal species from the high arctic1

“…This conclusion has been further supported by recent phylogenetic analyses of chloroplast and mitochondrial genomes (Turmel et al. ). The computed ITS2 secondary structure of the new Mantoniella strains contained the four helix domains found in many eukaryotic taxa (Fig.…”

The complete plastome of the coccoid green alga Jenufa minuta (Chlorophyceae, incertae sedis) unveils a noncanonical genetic code and a previously unrecognized trans-spliced group II intron in the rpl32 gene

“…In contrast, evidence for a variant genetic code (i.e. reassignment of AUA from isoleucine to methionine) in the plastome has been reported only for the tiny prasinophytes belonging to the genus Chloroparvula (Chloropicophyceae) (Turmel et al 2019). Here, we present the plastome sequence of Jenufa minuta (Chlorophyceae, incertae sedis) and provide evidence for a second case of noncanonical genetic code.…”

Elemental and macromolecular composition of the marine Chloropicophyceae, a major group of oceanic photosynthetic picoeukaryotes

“…Chlorophytes are among the most numerically dominant groups contributing to marine photosynthetic eukaryote communities in the less than 3‐ μ m size class (Simmons et al 2016; Tragin and Vaulot 2019). In coastal regions, Ostreococcus , Micromonas , and Bathycoccus , members of the class Mamiellophyceae, are often dominant contributors to photosynthetic picoeukaryote communities (Not et al 2004; Karlusich et al 2020), while in more oceanic regions, Chloropicon and Chloroparvula of the class Chloropicophyceae are more likely to be dominant constituents of photosynthetic picoeukaryotes communities (Lopes dos Santos et al 2017 a ,b; Turmel et al 2019). While there is some work on the physiology and elemental composition of Mamiellophyceae (Garcia et al 2018; Liefer et al 2019), data on the growth rate, elemental (C : N : P), and macromolecular composition of the Chloropicophyceae is lacking.…”