Genome of the red alga Porphyridium purpureum

Abstract

The limited knowledge we have about red algal genomes comes from the highly specialized extremophiles, Cyanidiophyceae. Here, we describe the first genome sequence from a mesophilic, unicellular red alga, Porphyridium purpureum. The 8,355 predicted genes in P. purpureum, hundreds of which are likely to be implicated in a history of horizontal gene transfer, reside in a genome of 19.7 Mbp with 235 spliceosomal introns. Analysis of light-harvesting complex proteins reveals a nuclear-encoded phycobiliprotein in the alga. We uncover a complex set of carbohydrate-active enzymes, identify the genes required for the methylerythritol phosphate pathway of isoprenoid biosynthesis, and find evidence of sexual reproduction. Analysis of the compact, function-rich genome of P. purpureum suggests that ancestral lineages of red algae acted as mediators of horizontal gene transfer between prokaryotes and photosynthetic eukaryotes, thereby significantly enriching genomes across the tree of photosynthetic life.

Figure 1. Analysis of the P. purpureum genome.

(a) Transmission electron microscopy image of a P. purpureum cell showing the central pyrenoid (Py), cell membrane (CM), starch granules (S) and plastid thylakoids (Th). (b) Percentage of single protein RAxML trees (raw numbers shown in the bars) that support the monophyly of P. purpureum (bootstrap ≥90%) solely with other Plantae members (exclusive), or in combination with non-Plantae taxa that interrupt this clade (non-exclusive). These latter groups of trees are primarily explained by red/green algal EGT into the nuclear genome of chromalveolates. For each of these algal lineages, the set of trees with different numbers of taxa (x) ≥4, ≥10, ≥20, ≥30 and ≥40 in a tree are shown. Each tree has ≥3 phyla. The Plantae-only groups are reds-greens-glaucophytes (RGGl) and reds-greens (RG).

Figure 2. Phylogenetic analysis of proteins on contig 2035b in P. purpureum.

These are all RAxML trees (WAG + Γ + I + F model) with the results of 100 bootstrap replicates shown on the branches. (a) Tree inferred from a squalene monooxygenase-like protein involved in sterol biosynthesis that shows the expected monophyly of red algae and of plants within the eukaryote tree of life. (b) Tree inferred from a tyrosine kinase/lipopolysaccharide-modifying enzyme that shows a complex phylogenetic relationship between red algae and chromalveolates. (c) Tree inferred from a glycosyltransferase of bacterial origin that is consistent with the monophyly of red algae and glaucophytes and a shared history of the gene in these taxa with chromalveolates, potentially via secondary EGT. (d) Tree inferred from an unknown protein in the aminotransferase superfamily that is present only in red algae and originated through HGT presumably from a proteobacterial source. The unit of branch length in each tree is the number of substitutions per site. The GenBank GI and Joint Genome Institute (JGI) accession codes (where available) are shown after each taxon name.

Figure 3. Analysis of a transporter in P. purpureum.

Schematic image showing the putative sodium–potassium ATPase and sodium:glucose cotransporter identified in the P. purpureum genome data.

Figure 4. Analysis of CYPs and sphingolipid metabolism in P. purpureum.

(a) Maximum likelihood (RAxML; LG + Γ + I + F model) tree of CYP sequences from P. purpureum and other eukaryotes. Support for internal branches was assessed using 100 bootstrap replicates. The major known CYP clans are indicated. (b) Putative sphingolipid synthesis pathway in P. purpureum deduced from analyses of vascular plants (for example, Arabidopsis). Modifications without candidate genes in the P. purpureum draft assembly are indicated in red. Cer, ceramide; GCS, glucosylceramide synthase; GIPC, glucosyl inositol phosphoryl ceramide; GlcCer, glucosylceramide; IPC, inositol phosphoryl ceramide; LCB, long chain base; and VLCFA, very long chain fatty acid.