Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida

Abstract

Red seaweeds are key components of coastal ecosystems and are economically important as food and as a source of gelling agents, but their genes and genomes have received little attention. Here we report the sequencing of the 105-Mbp genome of the florideophyte Chondrus crispus (Irish moss) and the annotation of the 9,606 genes. The genome features an unusual structure characterized by gene-dense regions surrounded by repeat-rich regions dominated by transposable elements. Despite its fairly large size, this genome shows features typical of compact genomes, e.g., on average only 0.3 introns per gene, short introns, low median distance between genes, small gene families, and no indication of large-scale genome duplication. The genome also gives insights into the metabolism of marine red algae and adaptations to the marine environment, including genes related to halogen metabolism, oxylipins, and multicellularity (microRNA processing and transcription factors). Particularly interesting are features related to carbohydrate metabolism, which include a minimalistic gene set for starch biosynthesis, the presence of cellulose synthases acquired before the primary endosymbiosis showing the polyphyly of cellulose synthesis in Archaeplastida, and cellulases absent in terrestrial plants as well as the occurrence of a mannosylglycerate synthase potentially originating from a marine bacterium. To explain the observations on genome structure and gene content, we propose an evolutionary scenario involving an ancestral red alga that was driven by early ecological forces to lose genes, introns, and intergenetic DNA; this loss was followed by an expansion of genome size as a consequence of activity of transposable elements.T he red algae, together with the glaucophytes and the Chloroplastida, are members of the Archaeplastida, the phylogenetic group formed during the primary endosymbiosis event that gave rise to the first photosynthetic eukaryote. Red algal genomes, both plastid and nuclear, also contributed, via secondary endosymbiosis, to several other eukaryotic lineages, including

Eukaryotic algal phytochromes span the visible spectrum

“…Indeed, phytochrome is absent in the rhodophyte (red alga) Chondrus crispus, found from intertidal regions to ∼20-m depth (20,21). Similarly, the green alga Chlamydomonas reinhardtii lacks phytochrome despite retaining the ability to synthesize the bilin chromophore phycocyanobilin (PCB) (22).…”

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

“…This contrasts with the relatively less complex TF repertoire of other multicellular lineages, such as Fungi, the brown algae E. siliculosus, or even the red alga Chondrus crispus (51). There exists the possibility that our analysis has missed as-yet-undescribed TFs that are unique to those lineages, as TFs that are restricted to small clades may be more prevalent than expected (52).…”

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

“…plants have lost these genes as a key adaptation to terrestrial as well as freshwater conditions 19,20 . In contrast, Z. marina has regained the ability to produce sulfated polysaccharides with an expansion of aryl sulfotransferases (12 genes) homologous to aryl sulfotransferases from land plants (Supplementary Note 10).…”