The inflated mitochondrial genomes of siphonous green algae reflect processes driving expansion of noncoding DNA and proliferation of introns

Abstract

Within the siphonous green algal order Bryopsidales, the size and gene arrangement of chloroplast genomes has been examined extensively, while mitochondrial genomes have been mostly overlooked. The recently published mitochondrial genome of Caulerpa lentillifera is large with expanded noncoding DNA, but it remains unclear if this is characteristic of the entire order. Our study aims to evaluate the evolutionary forces shaping organelle genome dynamics in the Bryopsidales based on the C. lentillifera and Ostreobium quekettii mitochondrial genomes. In this study, the mitochondrial genome of O. quekettii was characterised using a combination of long and short read sequencing, and bioinformatic tools for annotation and sequence analyses. We compared the mitochondrial and chloroplast genomes of O. quekettii and C. lentillifera to examine hypotheses related to genome evolution. The O. quekettii mitochondrial genome is the largest green algal mitochondrial genome sequenced (241,739 bp), considerably larger than its chloroplast genome. As with the mtDNA of C. lentillifera, most of this excess size is from the expansion of intergenic DNA and proliferation of introns. Inflated mitochondrial genomes in the Bryopsidales suggest effective population size, recombination and/or mutation rate, influenced by nuclear-encoded proteins, differ between the genomes of mitochondria and chloroplasts, reducing the strength of selection to influence evolution of their mitochondrial genomes.

Multiple Intraspecific Variations of Mitochondrial Genomes in the Green-Tide Forming Alga, Ulva compressa Linnaeus (Ulvophyceae, Chlorophyta)

“…The variation of U. compressa mitogenome size was mainly caused by differences in the content of genome-specific free-standing orf s (sfORFs), both group I and II introns, and the non-coding intergenic spacer regions (Figure 2). The content of non-coding spacer in U. compressa mitogenomes was 22.29-26.93% (Figure 2), which was within the known range for Ulva mitogenomes (20.51-32.94%), but was lower than the mitogenomes of Bryopsidales (34.8-46.0%) (Zheng et al, 2018;Repetti et al, 2020), Ulotrichales (43.3-49.0%) (Pombert et al, 2004;Turmel et al, 2016), and Oltmannsiellopsidales (34.1%) (Pombert et al, 2006), displaying the most compact architectures among the Ulvophyceae so far. The overall A + T content in the United States sample (Uco1) was 61.96%, which was the lowest value recorded in Ulva mitogenomes sequenced so far (Liu et al, 2017).…”

“…All of the genes annotated in Uco2-5 were coded on the same strand and shared a high level of conservation in gene synteny, as was the same as that in the other Ulva mitogenomes (Melton et al, 2015;Liu et al, 2017), but was different from the mitogenomes of Ulotrichales, Bryopsidales and Oltmannsiellopsidales which had their genes distributed on the two strands (Pombert et al, 2006;Turmel et al, 2016;Repetti et al, 2020). However, a locally collinear block of eight genes (rps11-rps19-rps4-rpl16-trnR-trnQ-trnE-trnS) with the size of 3,631 bp has been inverted only in Uco1 (Figure 6), indicating that this rearrangement event happened after its divergence from Uco2-5.…”

“…The reported ulvophycean mitogenomes exhibit large variation in genome size, architechtures, gene density, and intron content (Liu et al, 2017). Species in Bryopsidales harbor the inflated mitogenomes ranged from 197,427 bp in Caulerpa ashmeadii to 241,739 bp in Ostreobium quekettii, due to expansion of noncoding DNA and proliferation of introns (Sauvage et al, 2019;Repetti et al, 2020). Species in Ulotrichales tend to contain large mitogenomes, such as the 105,236-bp Gloeotilopsis planctonica and 95,880-bp Pseudendoclonium akinetum mitogenomes, which also display characteristics of the 'expanded-derived' patterns of evolution (Pombert et al, 2004;Turmel et al, 2016).…”

Genomic adaptations to an endolithic lifestyle in the coral-associated algaOstreobium

“…Transcriptome data of Ostreobium , assembled using Trinity v2.9.1 [65] in the de novo mode, were obtained from an earlier published work [66]. Using the genome assembly generated in this study, the transcriptome (RNA-Seq) reads (GenBank BioProject accession PRJEB35267) were assembled using Trinity in the “genome-guided” mode.…”

Common Repeat Elements in the Mitochondrial and Plastid Genomes of Green Algae

“…A common family of GC-rich repeat elements, many of which are palindromic (i.e., a sequences that can be folded into hairpin structures), have spread throughout the H. lacustris mtDNA and ptDNA, resulting in the unprecedented situation whereby these two different genomes are largely made up of matching sequences (Zhang et al, 2019). The proliferation of these elements has resulted in extremely high organelle GC compositions (∼50%) (Smith, 2012) as well as severe genome expansion-the plastome of H. lacustris, at 1.35 Mb, is the largest on record (Bauman et al, 2018;Smith, 2018) and its mtDNA (124.6 kb) is among the biggest from green algae (Zhang et al, 2019;Repetti et al, 2020).…”