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Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and genome organization.

Pérez-Brocal V, Clark CG - Mol. Biol. Evol. (2008)

Bottom Line: The human parasitic stramenopile Blastocystis is a rare example of an anaerobic eukaryote with organelles that have retained some mitochondrial characteristics, including a genome, whereas they lack others, such as cytochromes.Here we report the sequence and comparative analysis of the organellar genome from two different Blastocystis isolates as well as a comparison to other genomes from stramenopile mitochondria.Analysis of the characteristics displayed by the unique Blastocystis organelle genome gives us an insight into the initial evolutionary steps that may have led from mitochondria to hydrogenosomes and mitosomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom.

ABSTRACT
Acquisition of mitochondria by the ancestor of all living eukaryotes represented a crucial milestone in the evolution of the eukaryotic cell. Nevertheless, a number of anaerobic unicellular eukaryotes have secondarily discarded certain mitochondrial features, leading to modified organelles such as hydrogenosomes and mitosomes via degenerative evolution. These mitochondrion-derived organelles have lost many of the typical characteristics of aerobic mitochondria, including certain metabolic pathways, morphological traits, and, in most cases, the organellar genome. So far, the evolutionary pathway leading from aerobic mitochondria to anaerobic degenerate organelles has remained unclear due to the lack of examples representing intermediate stages. The human parasitic stramenopile Blastocystis is a rare example of an anaerobic eukaryote with organelles that have retained some mitochondrial characteristics, including a genome, whereas they lack others, such as cytochromes. Here we report the sequence and comparative analysis of the organellar genome from two different Blastocystis isolates as well as a comparison to other genomes from stramenopile mitochondria. Analysis of the characteristics displayed by the unique Blastocystis organelle genome gives us an insight into the initial evolutionary steps that may have led from mitochondria to hydrogenosomes and mitosomes.

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ML tree of nad proteins. This tree was obtained using the edited alignment produced by MUSCLE v. 3.6, the CpREV+I+G+F amino acid substitution model, and is based on the concatenated amino acid sequences of the nine NADH dehydrogenase genes present in all of the stramenopiles included (i.e., nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, and nad9; see Materials and Methods) as well as in the 12 taxa used as outgroups. Numbers beside the internal nodes are the ML bootstrap values from 400 resamplings obtained with Phyml and the Bayesian MCMC posterior probability values. Black circles indicate 100% bootstrap support and 1.00 posterior probability values. Support values over 50% are shown adjacent to the corresponding nodes. Values below 50% are represented by a dash (–). The clade containing all the stramenopiles is shaded. Taxonomic classification follows the nomenclature of Adl et al. (2005).
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fig2: ML tree of nad proteins. This tree was obtained using the edited alignment produced by MUSCLE v. 3.6, the CpREV+I+G+F amino acid substitution model, and is based on the concatenated amino acid sequences of the nine NADH dehydrogenase genes present in all of the stramenopiles included (i.e., nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, and nad9; see Materials and Methods) as well as in the 12 taxa used as outgroups. Numbers beside the internal nodes are the ML bootstrap values from 400 resamplings obtained with Phyml and the Bayesian MCMC posterior probability values. Black circles indicate 100% bootstrap support and 1.00 posterior probability values. Support values over 50% are shown adjacent to the corresponding nodes. Values below 50% are represented by a dash (–). The clade containing all the stramenopiles is shaded. Taxonomic classification follows the nomenclature of Adl et al. (2005).

Mentions: The ML tree based on the amino acid sequences of nine nad genes is shown in figure 2 (nad11 was excluded as it is not present in all organelle genomes analyzed). The topology of the Bayesian tree was identical. Trees using either method strongly support the clustering of Blastocystis sp. DMP/02-328 and NandII as a monophyletic clade, with weaker support for the Peronosporomycetes, represented by S. ferax and Phytophthora spp., as a sister group. This result suggests that oomycete mitochondrial genomes are the closest relatives of the Blastocystis MLO, in agreement with the analysis of Stechmann et al. (2008), which was based on a smaller number of MLO genes. Our trees support the monophyly of the Phaeophyceae, the Peronosporomycetes, and the clade consisting of the Chrysophyceae and Synurales. The branch lengths also agree with the relative rate test of substitution (Moran 1996; data not shown) in reflecting intermediate values of acceleration in substitution rates in Blastocystis sp., compared with the more accelerated C. roenbergensis and the slower remaining stramenopiles.


Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and genome organization.

Pérez-Brocal V, Clark CG - Mol. Biol. Evol. (2008)

ML tree of nad proteins. This tree was obtained using the edited alignment produced by MUSCLE v. 3.6, the CpREV+I+G+F amino acid substitution model, and is based on the concatenated amino acid sequences of the nine NADH dehydrogenase genes present in all of the stramenopiles included (i.e., nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, and nad9; see Materials and Methods) as well as in the 12 taxa used as outgroups. Numbers beside the internal nodes are the ML bootstrap values from 400 resamplings obtained with Phyml and the Bayesian MCMC posterior probability values. Black circles indicate 100% bootstrap support and 1.00 posterior probability values. Support values over 50% are shown adjacent to the corresponding nodes. Values below 50% are represented by a dash (–). The clade containing all the stramenopiles is shaded. Taxonomic classification follows the nomenclature of Adl et al. (2005).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2568035&req=5

fig2: ML tree of nad proteins. This tree was obtained using the edited alignment produced by MUSCLE v. 3.6, the CpREV+I+G+F amino acid substitution model, and is based on the concatenated amino acid sequences of the nine NADH dehydrogenase genes present in all of the stramenopiles included (i.e., nad1, nad2, nad3, nad4, nad4L, nad5, nad6, nad7, and nad9; see Materials and Methods) as well as in the 12 taxa used as outgroups. Numbers beside the internal nodes are the ML bootstrap values from 400 resamplings obtained with Phyml and the Bayesian MCMC posterior probability values. Black circles indicate 100% bootstrap support and 1.00 posterior probability values. Support values over 50% are shown adjacent to the corresponding nodes. Values below 50% are represented by a dash (–). The clade containing all the stramenopiles is shaded. Taxonomic classification follows the nomenclature of Adl et al. (2005).
Mentions: The ML tree based on the amino acid sequences of nine nad genes is shown in figure 2 (nad11 was excluded as it is not present in all organelle genomes analyzed). The topology of the Bayesian tree was identical. Trees using either method strongly support the clustering of Blastocystis sp. DMP/02-328 and NandII as a monophyletic clade, with weaker support for the Peronosporomycetes, represented by S. ferax and Phytophthora spp., as a sister group. This result suggests that oomycete mitochondrial genomes are the closest relatives of the Blastocystis MLO, in agreement with the analysis of Stechmann et al. (2008), which was based on a smaller number of MLO genes. Our trees support the monophyly of the Phaeophyceae, the Peronosporomycetes, and the clade consisting of the Chrysophyceae and Synurales. The branch lengths also agree with the relative rate test of substitution (Moran 1996; data not shown) in reflecting intermediate values of acceleration in substitution rates in Blastocystis sp., compared with the more accelerated C. roenbergensis and the slower remaining stramenopiles.

Bottom Line: The human parasitic stramenopile Blastocystis is a rare example of an anaerobic eukaryote with organelles that have retained some mitochondrial characteristics, including a genome, whereas they lack others, such as cytochromes.Here we report the sequence and comparative analysis of the organellar genome from two different Blastocystis isolates as well as a comparison to other genomes from stramenopile mitochondria.Analysis of the characteristics displayed by the unique Blastocystis organelle genome gives us an insight into the initial evolutionary steps that may have led from mitochondria to hydrogenosomes and mitosomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom.

ABSTRACT
Acquisition of mitochondria by the ancestor of all living eukaryotes represented a crucial milestone in the evolution of the eukaryotic cell. Nevertheless, a number of anaerobic unicellular eukaryotes have secondarily discarded certain mitochondrial features, leading to modified organelles such as hydrogenosomes and mitosomes via degenerative evolution. These mitochondrion-derived organelles have lost many of the typical characteristics of aerobic mitochondria, including certain metabolic pathways, morphological traits, and, in most cases, the organellar genome. So far, the evolutionary pathway leading from aerobic mitochondria to anaerobic degenerate organelles has remained unclear due to the lack of examples representing intermediate stages. The human parasitic stramenopile Blastocystis is a rare example of an anaerobic eukaryote with organelles that have retained some mitochondrial characteristics, including a genome, whereas they lack others, such as cytochromes. Here we report the sequence and comparative analysis of the organellar genome from two different Blastocystis isolates as well as a comparison to other genomes from stramenopile mitochondria. Analysis of the characteristics displayed by the unique Blastocystis organelle genome gives us an insight into the initial evolutionary steps that may have led from mitochondria to hydrogenosomes and mitosomes.

Show MeSH