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.

Experimental identification and in silico prediction of bacterivory in green algae

“…Furthermore, the model predicted three additional green algal taxa to be phago-mixotrophs, including Chloropicon primus, Crustomastix stigmatica , and Mesostigma viride . The dataset used for Chloropicon primus CCMP1205 is the first complete genome available for the recently characterized Chloropicophyceae [ 56 ]. This prediction is particularly surprising in that members of the Chloropicophyceae are small scale-less non-motile cells of 2–3 µm [ 57 ].…”

A streamlined and predominantly diploid genome in the tiny marine green alga Chloropicon primus

“…No polymorphisms were detected by mapping the sequencing reads generated in the course of this study against the 64.3-kb plastome and 37.9-kb mitogenome reference sequences available for C . primus 20,31 . Comparison of the coverage depth of PacBio subreads (449x and 253x for the plastome and mitogenome, respectively) to the mean PacBio sequencing depth obtained for the 19 chromosomes present in two copies (73×) enabled us to estimate that each Chloropicon cell, which contains a single chloroplast and a single mitochondrion, houses about 12 plastid and seven mitochondrial DNA molecules.…”

“…Recently, a late-diverging lineage of pico/nano-prasinophytes, named Chloropicophyceae, has emerged as playing a key role in marine phytoplankton communities, especially in moderately oligotrophic waters 29,30 . This genetically diversified lineage, which includes two genera ( Chloropicon and Chloroparvula ), occupies a sister position relative to the core Chlorophyta 2,20,30,31 (Fig. 1a) and although its members represent the dominant green algal group in open oceanic waters of tropical regions, little is known about their life cycle (sexual reproduction has not been observed) and their biochemical and physiological features.…”

Complete mitogenome of the chlorophyte green alga Marsupiomonas sp. NIES 1824 (Pedinophyceae)

“… 2017 ; Turmel, Lopes Dos Santos, et al. 2019 ; Turmel, Otis, et al. 2019 ), resembles the reduced mitogenomes of chlamydomonadalean algae (Chlorophyceae) (Turmel et al.…”