The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation

Abstract

Background: Little is known about the mechanisms of adaptation of life to the extreme environmental conditions encountered in polar regions. Here we present the genome sequence of a unicellular green alga from the division chlorophyta, Coccomyxa subellipsoidea C-169, which we will hereafter refer to as C-169. This is the first eukaryotic microorganism from a polar environment to have its genome sequenced.

Results: The 48.8 Mb genome contained in 20 chromosomes exhibits significant synteny conservation with the chromosomes of its relatives Chlorella variabilis and Chlamydomonas reinhardtii. The order of the genes is highly reshuffled within synteny blocks, suggesting that intra-chromosomal rearrangements were more prevalent than inter-chromosomal rearrangements. Remarkably, Zepp retrotransposons occur in clusters of nested elements with strictly one cluster per chromosome probably residing at the centromere. Several protein families overrepresented in C. subellipsoidae include proteins involved in lipid metabolism, transporters, cellulose synthases and short alcohol dehydrogenases. Conversely, C-169 lacks proteins that exist in all other sequenced chlorophytes, including components of the glycosyl phosphatidyl inositol anchoring system, pyruvate phosphate dikinase and the photosystem 1 reaction center subunit N (PsaN).

Conclusions: We suggest that some of these gene losses and gains could have contributed to adaptation to low temperatures. Comparison of these genomic features with the adaptive strategies of psychrophilic microbes suggests that prokaryotes and eukaryotes followed comparable evolutionary routes to adapt to cold environments.

Figure 1

Venn diagram showing unique and shared gene families between and among three sequenced chlorophyte species (Coccomyxa subellipsoidea C-169, Chlorella variabilis NC64A, and Chlamydomonas reinhardtii). Numbers of gene families are indicated in black. Total numbers of genes included in gene families are indicated in blue.

Figure 2

Levels of conserved synteny between green algae. (a) Dot-plot of 5,232 putative orthologous genes in the genome assemblies of C-169 and C. variabilis. Red and green dots show orthologous genes on the same and opposite strands, respectively. The width and length of each box are proportional to the lengths (bp) of the scaffolds determining the box. Scaffolds are organized in decreasing size order. The background color of boxes reflects the statistical significance (Z-score) of the number of orthologous genes (that is, conservation of synteny) shared between pairs of scaffolds relative to a non-syntenic model. The figure shows only the 29 biggest scaffolds of each species. (b) Numbers of conserved adjacent gene pairs and synteny correlation coefficients between pairs of sequenced chlorophytes appearing in the phylogenetic tree shown on the left. The maximum likelihood phylogenetic tree of sequenced chlorophytes was computed with the WAG+G+I model from a concatenated alignment of 1,253 orthologous proteins totaling 263,131 gap-free sites. The upper half of the matrix shows the levels of synteny conservation between pairs of genome assemblies as measured by the synteny correlation coefficient [17]. The lower half shows the numbers of pairs of orthologous genes that are adjacent in two genome assemblies. The background color of boxes reflects the statistical significance (Z-score) of the synteny correlation coefficient (blue) and number of conserved adjacent gene pairs (orange) relative to a non-syntenic model. Olu, Ostreococcus lucimarinus; ORCC, Ostreococcus sp. RCC809; Ota, Ostreococcus tauri; MRCC, Micromonas sp. RCC299; MCCMP, Micromonas pusilla CCMP1545; Crei, Chlamydomonas reinhardtii; Vcar, Volvox carteri; Chlo, Chlorella variabilis NC64A; Cocco, Coccomyxa subellipsoidea C-169.

Figure 3

Maximum likelihood phylogenetic tree of the ketoacyl-ACP synthase (KAS) domains and proteins of fatty acid synthases (FASs) and polyketide synthases (PKSs). The phylogenetic tree was constructed using the WAG+G+I substitution model. The multiple-alignment contained 274 gap-free columns. Approximate likelihood ratio test (aLRT) values for branch support are indicated beside branches when aLRT > 50. GenBank accession numbers and protein ids (C-169) are indicated between brackets. For C-169 proteins, the number of ESTs corresponding to the gene is shown in red. The branch length scale bar below the phylogenetic tree indicates the number of substitutions per amino acid site. The functional domain architecture of proteins is shown on the right. Protein domain names are as follows: ACP, acyl carrier protein; AT, acyl transferase; DH, hydroxyacyl-ACP dehydrase; ER, enoyl-ACP reductase; KAS, ketoacyl-ACP synthase; KR, ketoacyl-ACP reductase; MT, methyltransferase; NRPS, non-ribosomal protein synthase terminal domain; PPT, phosphopantetheinyl transferase; TE, thioesterase.