Proliferation of group II introns in the chloroplast genome of the green algaOedocladium carolinianum(Chlorophyceae)

Abstract

BackgroundThe chloroplast genome sustained extensive changes in architecture during the evolution of the Chlorophyceae, a morphologically and ecologically diverse class of green algae belonging to the Chlorophyta; however, the forces driving these changes are poorly understood. The five orders recognized in the Chlorophyceae form two major clades: the CS clade consisting of the Chlamydomonadales and Sphaeropleales, and the OCC clade consisting of the Oedogoniales, Chaetophorales, and Chaetopeltidales. In the OCC clade, considerable variations in chloroplast DNA (cpDNA) structure, size, gene order, and intron content have been observed. The large inverted repeat (IR), an ancestral feature characteristic of most green plants, is present in Oedogonium cardiacum (Oedogoniales) but is lacking in the examined members of the Chaetophorales and Chaetopeltidales. Remarkably, the Oedogonium 35.5-kb IR houses genes that were putatively acquired through horizontal DNA transfer. To better understand the dynamics of chloroplast genome evolution in the Oedogoniales, we analyzed the cpDNA of a second representative of this order, Oedocladium carolinianum.MethodsThe Oedocladium cpDNA was sequenced and annotated. The evolutionary distances separating Oedocladium and Oedogonium cpDNAs and two other pairs of chlorophycean cpDNAs were estimated using a 61-gene data set. Phylogenetic analysis of an alignment of group IIA introns from members of the OCC clade was performed. Secondary structures and insertion sites of oedogonialean group IIA introns were analyzed.ResultsThe 204,438-bp Oedocladium genome is 7.9 kb larger than the Oedogonium genome, but its repertoire of conserved genes is remarkably similar and gene order differs by only one reversal. Although the 23.7-kb IR is missing the putative foreign genes found in Oedogonium, it contains sequences coding for a putative phage or bacterial DNA primase and a hypothetical protein. Intergenic sequences are 1.5-fold longer and dispersed repeats are more abundant, but a smaller fraction of the Oedocladium genome is occupied by introns. Six additional group II introns are present, five of which lack ORFs and carry highly similar sequences to that of the ORF-less IIA intron shared with Oedogonium. Secondary structure analysis of the group IIA introns disclosed marked differences in the exon-binding sites; however, each intron showed perfect or nearly perfect base pairing interactions with its target site.DiscussionOur results suggest that chloroplast genes rearrange more slowly in the Oedogoniales than in the Chaetophorales and raise questions as to what was the nature of the foreign coding sequences in the IR of the common ancestor of the Oedogoniales. They provide the first evidence for intragenomic proliferation of group IIA introns in the Viridiplantae, revealing that intron spread in the Oedocladium lineage likely occurred by retrohoming after sequence divergence of the exon-binding sites.

The chloroplast genome of the lichen‐symbiont microalga Trebouxia sp. Tr9 (Trebouxiophyceae, Chlorophyta) shows short inverted repeats with a single gene and loss of the rps4 gene, which is encoded by the nucleus

“…The presence of similar ncORFs in distant algal lineages, such as the Chlorophyceae (Brouard et al. ), Prasinophyceae (Lemieux et al. 2014b), and Trebouxiophyceae (this study, and Turmel et al.…”

“…], Oedogonium cardiacum and Oedocladium carolinianun [Chlorophyceae; Brouard et al. , ], Parachlorella kessleri [Trebouxiophyceae; Turmel et al. 2009b], and Entransia fimbriata [Streptophyta, Turmel et al.…”

Chloroplast genome expansion by intron multiplication in the basal psychrophilic euglenoidEutreptiella pomquetensis

“…This would provide an accessible splicing apparatus and allow all but one intron to lose its own IEP ( Dai & Zimmerly, 2003 ; Lambowitz & Belfort, 2015 ; Lambowitz & Zimmerly, 2011 ). Brouard et al (2016) assumed that the freestanding orf1311 in Oedocladium (Chlorophyceae), with an intron encoded maturase, could function as promoter for splicing the ORF-less group II introns. Turmel, Otis & Lemieux (2016) detected introns in G. planctonica without ORFs, which may reflect an evolutionary pressure for a smaller and more compact intron structure enabling increased efficiency of splicing and mobility, when maturase activity is provided from elsewhere.…”

“…Also, outside of euglenoid chloroplast introns, very few species showed high pairwise similarity. For instance, Brouard et al (2016) found six group IIA introns in the chlorophyte Oedocladium carolinianum with high levels of nucleotide identities, which displayed over 80% pairwise identity. As well Turmel, Otis & Lemieux (2016) found several group II introns with high nucleotide identities also at various insertion sites, but only in small numbers.…”

Mobile Group II Introns as Ancestral Eukaryotic Elements

“…Group II introns are actively involved in shaping their host genomes via mobility and horizontal transfer. Indeed, waves of group II intron proliferation were reported for some green algae [51, 52]. A remarkable example of intron propagation was found in cpDNA of the freshwater euglenid Euglena gracilis with almost all of its protein-coding genes interrupted [53].…”