Independent Size Expansions and Intron Proliferation in Red Algal Plastid and Mitochondrial Genomes

Abstract

Proliferation of selfish genetic elements has led to significant genome size expansion in plastid and mitochondrial genomes of various eukaryotic lineages. Within the red algae, such expansion events are only known in the plastid genomes of the Proteorhodophytina, a highly diverse group of mesophilic microalgae. By contrast, they have never been described in the much understudied red algal mitochondrial genomes. Therefore, it remains unclear how widespread such organellar genome expansion events are in this eukaryotic phylum. Here, we describe new mitochondrial and plastid genomes from 25 red algal species, thereby substantially expanding the amount of organellar sequence data available, especially for Proteorhodophytina, and show that genome expansions are common in this group. We confirm that large plastid genomes are limited to the classes Rhodellophyceae and Porphyridiophyceae, which in part are caused by lineage-specific expansion events. Independently expanded mitochondrial genomes - up to three times larger than typical red algal mitogenomes - occur across Proteorhodophytina classes and a large shift towards high GC content occurred in the Stylonematophyceae. Although intron proliferation is the main cause of plastid and mitochondrial genome expansion in red algae, we do not observe recent intron transfer between different organelles. Phylogenomic analyses of mitochondrial and plastid genes from our expanded taxon sampling yielded well-resolved phylogenies of red algae with strong support for the monophyly of Proteorhodophytina. Our work shows that organellar genomes followed different evolutionary dynamics across red algal lineages.

Red macroalgae in the genomic era

“…Molecular phylogenies have confirmed this traditional taxonomic separation and have grouped these two multicellular classes together in the subphyllum Eurhodophytina (Fig. 1), with the Bangiophyceae assemblage appearing to have paraphyletic origins (Yoon et al, 2006;Verbruggen et al, 2010;Qiu, 2016;Muñoz-G omez et al, 2017;Van Beveren et al, 2022). The other two Rhodophyta subphyla correspond to divergent ancient lineages that arose at the beginning of the Mesoproterozoic (c. 1500 million years ago (Ma)): the Cyanidiophytina, which contain thermoacidophilic unicellular red algae (Janou skovec et al, 2013), and the Proteorhodophytina, which are mainly unicellular but sometimes exhibit simple multicellular forms (Yoon et al, 2006).…”

“…Molecular phylogenies have confirmed this traditional taxonomic separation and have grouped these two multicellular classes together in the subphyllum Eurhodophytina (Fig. 1), with the Bangiophyceae assemblage appearing to have paraphyletic origins (Yoon et al ., 2006; Verbruggen et al ., 2010; Qiu, 2016; Muñoz‐Gómez et al ., 2017; Van Beveren et al ., 2022). The other two Rhodophyta subphyla correspond to divergent ancient lineages that arose at the beginning of the Mesoproterozoic ( c .…”

Nucleomorph phylogenomics suggests a deep and ancient origin of cryptophyte plastids within Rhodophyta

“…However, our insufficient understanding of phylogenetic relationships between red algal groups, as well as poor taxon sampling of rhodophyte genomes, have for a long time limited the usefulness of such studies in precisely pinpointing the donor taxon. Recent large-scale phylogenomic analyses of plastid-and mitochondrion-encoded genes (Muñoz-Gómez et al 2017;van Beveren et al 2022) have greatly advanced our understanding of the internal phylogeny of the phylum Rhodophyta. To attempt to phylogenetically place CASH plastids within the tree of Rhodophyta, we used an alternative source of genetic data -the nucleomorph genomes of Cryptophyta (Cryptista).…”

The complete mitochondrial genome of Isochrysis galbana harbors a unique repeat structure and a specific trans-spliced cox1 gene

“…( Nishimura et al, 2014 ) and Phaeocystis globosa ( Song et al, 2021 ) from Prymnesiales, Pavlova lutheri ( Hulatt et al, 2020 ) and Diacronema viridis ( Kim et al, 2021 ) from Pavlovales, and a novel alga Pavlomulina ranunculiformis NIES-3900 from a newly erected haptophyte class, Rappephyceae ( Kawachi et al, 2021 ). The small mitogenome has been considered as an ideal model for genetic diversity, phylogenetic and comparative genomic analysis in algal species with improved resolution compared with traditional molecular markers ( Kim et al, 2018 ; Sibbald et al, 2021 ; Starko et al, 2021 ; Zhang et al, 2021 ; Van Beveren et al, 2022 ). Unveiling more haptophyte mitogenomes would provide insight into the evolutionary history of haptophytes and the relationships among CASH lineages.…”

“…The first full-length mitogenome of haptophyte P. globosa strain CNS00066 contains two large repeat regions with combined length of 20.7 kb, representing the longest repeat region among sequenced haptophytes mitogenomes ( Song et al, 2021 ). The accumulation of tandem repeats in large intergenic regions (LIRs) of mitogenomes are also ubiquitous in unicellular green algae ( Turmel et al, 1999 , 2007 ), red algae ( Van Beveren et al, 2022 ), cryptophytes ( Hauth et al, 2005 ; Kim et al, 2008 ) and diatoms ( Oudot-Le Secq and Green, 2011 ). Porphyridium harbors the largest red algal mitogenomes reported thus far, which could be ascribed to the invasion of group II introns in genic regions and the repeat-rich LIRs ( Kim et al, 2022 ).…”