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The mitochondrial genome of the entomoparasitic green alga helicosporidium.

Pombert JF, Keeling PJ - PLoS ONE (2010)

Bottom Line: The complete plastid genome of an Helicosporidium species was recently described and is a model of compaction and reduction.The architecture, genome content, and phylogeny of the Helicosporidium mitochondrial genome are all congruent with its close relationship to Prototheca within the Trebouxiophyceae.The Helicosporidium mitochondrial genome does, however, contain a number of novel features, particularly relating to its introns.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada. jpombert@interchange.ubc.ca

ABSTRACT

Background: Helicosporidia are achlorophyllous, non-photosynthetic protists that are obligate parasites of invertebrates. Highly specialized, these pathogens feature an unusual cyst stage that dehisces inside the infected organism and releases a filamentous cell displaying surface projections, which will penetrate the host gut wall and eventually reproduce in the hemolymph. Long classified as incertae sedis or as relatives of other parasites such as Apicomplexa or Microsporidia, the Helicosporidia were surprisingly identified through molecular phylogeny as belonging to the Chlorophyta, a phylum of green algae. Most phylogenetic analyses involving Helicosporidia have placed them within the subgroup Trebouxiophyceae and further suggested a close affiliation between the Helicosporidia and the genus Prototheca. Prototheca species are also achlorophyllous and pathogenic, but they infect vertebrate hosts, inducing protothecosis in humans. The complete plastid genome of an Helicosporidium species was recently described and is a model of compaction and reduction. Here we describe the complete mitochondrial genome sequence of the same strain, Helicosporidium sp. ATCC 50920 isolated from the black fly Simulium jonesi.

Methodology/principal findings: The circular mapping 49343 bp mitochondrial genome of Helicosporidium closely resembles that of the vertebrate parasite Prototheca wickerhamii. The two genomes share an almost identical gene complement and display a level of synteny that is higher than any other sequenced chlorophyte mitochondrial DNAs. Interestingly, the Helicosporidium mtDNA feature a trans-spliced group I intron, and a second group I intron that contains two open reading frames that appear to be degenerate maturase/endonuclease genes, both rare characteristics for this type of intron.

Conclusions/significance: The architecture, genome content, and phylogeny of the Helicosporidium mitochondrial genome are all congruent with its close relationship to Prototheca within the Trebouxiophyceae. The Helicosporidium mitochondrial genome does, however, contain a number of novel features, particularly relating to its introns.

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Gene map of Helicosporidium mtDNA.Genes (filled boxes) located outside/inside the map are transcribed clockwise/counterclockwise. Introns are denoted by open boxes whereas intronic ORFs are illustrated as half-height boxes within the open boxes. tRNA genes are indicated by the one-letter amino acid code followed by the anticodon in parentheses (Me, elongator methionine; Mf, initiator methionine). ORFs smaller than 150 amino acids are not shown. Shared clusters between the Helicosporidium and Prototheca mitochondrial genomes are denoted by alterning black and gray brackets.
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pone-0008954-g001: Gene map of Helicosporidium mtDNA.Genes (filled boxes) located outside/inside the map are transcribed clockwise/counterclockwise. Introns are denoted by open boxes whereas intronic ORFs are illustrated as half-height boxes within the open boxes. tRNA genes are indicated by the one-letter amino acid code followed by the anticodon in parentheses (Me, elongator methionine; Mf, initiator methionine). ORFs smaller than 150 amino acids are not shown. Shared clusters between the Helicosporidium and Prototheca mitochondrial genomes are denoted by alterning black and gray brackets.

Mentions: The mitochondrial genome maps as a circular molecule of 49343 bp (Figure 1) featuring an overall A+T content of 74.4% (Table 1). The 60 genes it encodes are distributed with a marked strand polarity, but are not as symmetrical as those of Prototheca. The Helicosporidium mtDNA contains a total of four introns, all group I, which split the rnl and cox1 genes in three exons each. The Helicosporidium mtDNA also features three intronic open reading frames (ORFs) and two freestanding ORFs that are longer than 150 codons. Intergenic regions in the Helicosporidium mitochondrial genome range from 0 to 2355 bp, with an average of 183 bp, and no overlapping genes. The Helicosporidium mtDNA is more densely packed than that of Prototheca and is leaner by about 6 kbp despite maintaining a near-identical gene complement, differing only by a single tRNA, trnG(gcc) (Tables S1 and S2). Both genomes features trnT(ugu), a tRNA-encoding gene also found within the mtDNA of the ulvophycean alga Pseudendoclonium (Table S2). Like Prototheca and Pseudendoclonium mtDNAs, the Helicosporidium mitochondrial genome harbors a self-sufficient tRNA gene complement able to decode all codons assuming super Wobble codon/anticodon interactions. Codon usage in Helicosporidium mtDNA (Table S3) is also similar to that of Prototheca mtDNA, which parallels their very similar A+T content.


The mitochondrial genome of the entomoparasitic green alga helicosporidium.

Pombert JF, Keeling PJ - PLoS ONE (2010)

Gene map of Helicosporidium mtDNA.Genes (filled boxes) located outside/inside the map are transcribed clockwise/counterclockwise. Introns are denoted by open boxes whereas intronic ORFs are illustrated as half-height boxes within the open boxes. tRNA genes are indicated by the one-letter amino acid code followed by the anticodon in parentheses (Me, elongator methionine; Mf, initiator methionine). ORFs smaller than 150 amino acids are not shown. Shared clusters between the Helicosporidium and Prototheca mitochondrial genomes are denoted by alterning black and gray brackets.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2813288&req=5

pone-0008954-g001: Gene map of Helicosporidium mtDNA.Genes (filled boxes) located outside/inside the map are transcribed clockwise/counterclockwise. Introns are denoted by open boxes whereas intronic ORFs are illustrated as half-height boxes within the open boxes. tRNA genes are indicated by the one-letter amino acid code followed by the anticodon in parentheses (Me, elongator methionine; Mf, initiator methionine). ORFs smaller than 150 amino acids are not shown. Shared clusters between the Helicosporidium and Prototheca mitochondrial genomes are denoted by alterning black and gray brackets.
Mentions: The mitochondrial genome maps as a circular molecule of 49343 bp (Figure 1) featuring an overall A+T content of 74.4% (Table 1). The 60 genes it encodes are distributed with a marked strand polarity, but are not as symmetrical as those of Prototheca. The Helicosporidium mtDNA contains a total of four introns, all group I, which split the rnl and cox1 genes in three exons each. The Helicosporidium mtDNA also features three intronic open reading frames (ORFs) and two freestanding ORFs that are longer than 150 codons. Intergenic regions in the Helicosporidium mitochondrial genome range from 0 to 2355 bp, with an average of 183 bp, and no overlapping genes. The Helicosporidium mtDNA is more densely packed than that of Prototheca and is leaner by about 6 kbp despite maintaining a near-identical gene complement, differing only by a single tRNA, trnG(gcc) (Tables S1 and S2). Both genomes features trnT(ugu), a tRNA-encoding gene also found within the mtDNA of the ulvophycean alga Pseudendoclonium (Table S2). Like Prototheca and Pseudendoclonium mtDNAs, the Helicosporidium mitochondrial genome harbors a self-sufficient tRNA gene complement able to decode all codons assuming super Wobble codon/anticodon interactions. Codon usage in Helicosporidium mtDNA (Table S3) is also similar to that of Prototheca mtDNA, which parallels their very similar A+T content.

Bottom Line: The complete plastid genome of an Helicosporidium species was recently described and is a model of compaction and reduction.The architecture, genome content, and phylogeny of the Helicosporidium mitochondrial genome are all congruent with its close relationship to Prototheca within the Trebouxiophyceae.The Helicosporidium mitochondrial genome does, however, contain a number of novel features, particularly relating to its introns.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada. jpombert@interchange.ubc.ca

ABSTRACT

Background: Helicosporidia are achlorophyllous, non-photosynthetic protists that are obligate parasites of invertebrates. Highly specialized, these pathogens feature an unusual cyst stage that dehisces inside the infected organism and releases a filamentous cell displaying surface projections, which will penetrate the host gut wall and eventually reproduce in the hemolymph. Long classified as incertae sedis or as relatives of other parasites such as Apicomplexa or Microsporidia, the Helicosporidia were surprisingly identified through molecular phylogeny as belonging to the Chlorophyta, a phylum of green algae. Most phylogenetic analyses involving Helicosporidia have placed them within the subgroup Trebouxiophyceae and further suggested a close affiliation between the Helicosporidia and the genus Prototheca. Prototheca species are also achlorophyllous and pathogenic, but they infect vertebrate hosts, inducing protothecosis in humans. The complete plastid genome of an Helicosporidium species was recently described and is a model of compaction and reduction. Here we describe the complete mitochondrial genome sequence of the same strain, Helicosporidium sp. ATCC 50920 isolated from the black fly Simulium jonesi.

Methodology/principal findings: The circular mapping 49343 bp mitochondrial genome of Helicosporidium closely resembles that of the vertebrate parasite Prototheca wickerhamii. The two genomes share an almost identical gene complement and display a level of synteny that is higher than any other sequenced chlorophyte mitochondrial DNAs. Interestingly, the Helicosporidium mtDNA feature a trans-spliced group I intron, and a second group I intron that contains two open reading frames that appear to be degenerate maturase/endonuclease genes, both rare characteristics for this type of intron.

Conclusions/significance: The architecture, genome content, and phylogeny of the Helicosporidium mitochondrial genome are all congruent with its close relationship to Prototheca within the Trebouxiophyceae. The Helicosporidium mitochondrial genome does, however, contain a number of novel features, particularly relating to its introns.

Show MeSH
Related in: MedlinePlus