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. 2009 Nov 13:1:439-48.
doi: 10.1093/gbe/evp047.

The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate

Natalie Donaher  1 , Goro Tanifuji, Naoko T Onodera, Stephanie A Malfatti, Patrick S G Chain, Yoshiaki Hara, John M Archibald
Affiliations

The complete plastid genome sequence of the secondarily nonphotosynthetic alga Cryptomonas paramecium: reduction, compaction, and accelerated evolutionary rate

Natalie Donaher et al. Genome Biol Evol. .

Abstract

The cryptomonads are a group of unicellular algae that acquired photosynthesis through the engulfment of a red algal cell, a process called secondary endosymbiosis. Here, we present the complete plastid genome sequence of the secondarily nonphotosynthetic species Cryptomonas paramecium CCAP977/2a. The approximately 78 kilobase pair (Kbp) C. paramecium genome contains 82 predicted protein genes, 29 transfer RNA genes, and a single pseudogene (atpF). The C. paramecium plastid genome is approximately 50 Kbp smaller than those of the photosynthetic cryptomonads Guillardia theta and Rhodomonas salina; 71 genes present in the G. theta and/or R. salina plastid genomes are missing in C. paramecium. The pet, psa, and psb photosynthetic gene families are almost entirely absent. Interestingly, the ribosomal RNA operon, present as inverted repeats in most plastid genomes (including G. theta and R. salina), exists as a single copy in C. paramecium. The G + C content (38%) is higher in C. paramecium than in other cryptomonad plastid genomes, and C. paramecium plastid genes are characterized by significantly different codon usage patterns and increased evolutionary rates. The content and structure of the C. paramecium plastid genome provides insight into the changes associated with recent loss of photosynthesis in a predominantly photosynthetic group of algae and reveals features shared with the plastid genomes of other secondarily nonphotosynthetic eukaryotes.

Keywords: cryptomonads; genome reduction; photosynthesis; plastids; secondary endosymbiosis.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
A circular mapping diagram of the plastid genome of Cryptomonas paramecium CCAP977/2a. The 77,717 bp genome contains a single rRNA operon, 82 predicted protein genes, and 29 tRNA genes. Genes shown on the outside of the circle are transcribed clockwise. Annotated genes are colored according to the functional categories shown in the lower right.
F<sc>IG</sc>. 2.—
FIG. 2.—
Representative inversions and deletions in the plastid genome of Cryptomonas paramecium. A large region of gene synteny shared between the genomes of the photosynthetic cryptomonads Guillardia theta and Rhodomonas salina is shown aligned with the single ribosomal operon-containing region of the C. paramecium genome. Genes in black are oriented left-to-right, those in red right-to-left. Blocks of synteny are highlighted, as are inversions between C. paramecium and G. theta/R. salina. tRNA genes are not shown for simplicity, with the exception of those within the rRNA operon.
F<sc>IG</sc>. 3.—
FIG. 3.—
Gene loss and maintenance of synteny in the Cryptomonas paramecium plastid genome. A syntenic region of the genome shared between the photosynthetic cryptomonad Guillardia theta (left) and the nonphotosynthetic cryptomonad C. paramecium (right) is shown. Genes are colored according to their functional category. The diagram represents approximately 10 kbp of the C. paramecium genome (individual genes are not shown to scale).
F<sc>IG</sc>. 4.—
FIG. 4.—
Maximum likelihood phylogenetic tree showing the position of the nonphotosynthetic cryptomonad Cryptomonas paramecium. The tree was constructed using RaxML from a supermatrix of 22 proteins and 5,076 unambiguously aligned amino acid positions (see Materials and Methods). Rapid bootstrap values (300 replicates) are shown. The primary and secondary plastid-containing algae are rooted with a single cyanobacterial sequence. The scale bar shows the inferred number of amino acid substitutions per site.
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