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.

Fig. 1.

Structural features of the Chondrus crispus (Cc) genome. (A) Percentage of genes with introns as a function of genome size in selected eukaryotes. (B) Gene density as a function of clustering in selected eukaryotes. Species: Ostreococcus lucimarinus (Ol), Cyanidioschyzon merolae (Cm), Micromonas pusilla (Mp), Saccharomyces cerevisiae (Sc), Phaeodactylum tricornutum (Pht), Leishmania major (Lm), Thalassiosira pseudonana (Tp), Phytophthora ramorum (Pr), Paramecium tetraurelia (Pt), Phytophthora sojae (Ps), Caenorhabditis elegans (Ce), Chlamydomonas reinhardtii (Cr), Arabidopsis thaliana (At), Ectocarpus siliculosus (Es), Oryza sativa (Os), Physcomitrella patens (Pp), Vitis vinifera (Vv), Sorghum bicolor (Sb), Gallus gallus (Gg), Danio rerio (Dr), Zea mays (Zm), Homo sapiens (Hs). Green symbols indicate chloroplastides; red, rhodophytes; blue, opisthokonts; brown, stramenopiles; and black, others.

Fig. 2.

Orthology groups within red algal protein-coding genes. The Venn diagram shows the ortholog groups identified within the genomes of C. crispus and Cyanidioschyzon merolae and within the available sequences of Calliarthron tuberculosum, P. cruentum, and Pyropia (Porphyra) yezoensis.

Fig. 3.

Phylogenetic trees of the cellulose synthases CESA and cellulose synthase-like proteins CSL (family GT2) and of the cellulases of the GH5 and GH45 families. All phylogenetic trees were constructed using the maximum likelihood (ML) approach with the program MEGA 5.05 (www.megasoftware.net). Numbers indicate the bootstrap values in the ML analysis.

Fig. 4.

Proposed scenario for the evolution of red algae. An ancestor with flagella and an intron-rich genome invaded an extreme environment, possibly acidic and high temperature, with a strong selection pressure toward a reduced genome, where a genome reduction took place. The red algae later recolonized the marine and freshwater environments and experienced an expansion of the genome through the activity of transposable elements. They now are represented by the florideophytes and the bangiophytes (red algae that are neither Cyanidiales nor florideophytes). Red ovals represent plastids; light blue circles, nucleus with ancestral genes; yellow, transposable elements.

Fig. 5.

Snapshot of the C. crispus genome analysis and an outline of the contents of the SI Appendix.