Dataset Information

Lateral gene transfer and gene duplication played a key role in the evolution of Mastigamoeba balamuthi hydrogenosomes.

ABSTRACT: Lateral gene transfer (LGT) is an important mechanism of evolution for protists adapting to oxygen-poor environments. Specifically, modifications of energy metabolism in anaerobic forms of mitochondria (e.g., hydrogenosomes) are likely to have been associated with gene transfer from prokaryotes. An interesting question is whether the products of transferred genes were directly targeted into the ancestral organelle or initially operated in the cytosol and subsequently acquired organelle-targeting sequences. Here, we identified key enzymes of hydrogenosomal metabolism in the free-living anaerobic amoebozoan Mastigamoeba balamuthi and analyzed their cellular localizations, enzymatic activities, and evolutionary histories. Additionally, we characterized 1) several canonical mitochondrial components including respiratory complex II and the glycine cleavage system, 2) enzymes associated with anaerobic energy metabolism, including an unusual D-lactate dehydrogenase and acetyl CoA synthase, and 3) a sulfate activation pathway. Intriguingly, components of anaerobic energy metabolism are present in at least two gene copies. For each component, one copy possesses an mitochondrial targeting sequence (MTS), whereas the other lacks an MTS, yielding parallel cytosolic and hydrogenosomal extended glycolysis pathways. Experimentally, we confirmed that the organelle targeting of several proteins is fully dependent on the MTS. Phylogenetic analysis of all extended glycolysis components suggested that these components were acquired by LGT. We propose that the transformation from an ancestral organelle to a hydrogenosome in the M. balamuthi lineage involved the lateral acquisition of genes encoding extended glycolysis enzymes that initially operated in the cytosol and that established a parallel hydrogenosomal pathway after gene duplication and MTS acquisition.

SUBMITTER: Nyvltova E

PROVIDER: S-EPMC4379409 | biostudies-literature | 2015 Apr

REPOSITORIES: biostudies-literature

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Lateral gene transfer and gene duplication played a key role in the evolution of Mastigamoeba balamuthi hydrogenosomes.

Nývltová Eva E Stairs Courtney W CW Hrdý Ivan I Rídl Jakub J Mach Jan J Pačes Jan J Roger Andrew J AJ Tachezy Jan J

Molecular biology and evolution 20150107 4

Lateral gene transfer (LGT) is an important mechanism of evolution for protists adapting to oxygen-poor environments. Specifically, modifications of energy metabolism in anaerobic forms of mitochondria (e.g., hydrogenosomes) are likely to have been associated with gene transfer from prokaryotes. An interesting question is whether the products of transferred genes were directly targeted into the ancestral organelle or initially operated in the cytosol and subsequently acquired organelle-targeting ...[more]

PMID: 25573905

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Project description:BackgroundLarge scale genome arrangement, such as whole gene insertion/deletion, plays an important role in bacterial genome evolution. Various methods have been employed to study the dynamic process of gene insertions and deletions, such as parsimony methods and maximum likelihood methods. Previous maximum likelihood studies have assumed that the rate of gene insertions/deletions is constant over different genes. This assumption is unrealistic. For instance, it has been shown that informational genes are less likely to be laterally transferred than non-informational genes. However, how much of the variation in gene transfer rates is due to the difference between informational genes and non-informational genes is unclear. In this study, a Gamma-distribution was incorporated in the likelihood estimation by considering rate variation for gene insertions/deletions between genes. This makes it possible to address whether a difference between informational genes and non-informational genes is the main contributor to rate variation of lateral gene transfers.ResultsThe results show that models incorporating rate variation fit the data better than do constant rate models in many phylogenetic groups. Even though informational genes are less likely to be laterally transferred than non-informational genes, the degree of rate variation for insertions/deletions did not change dramatically and remained high even when informational genes were excluded from the study. This suggests that the variation in rate of insertions/deletions is not due mainly to the simple difference between informational genes and non-informational genes. Among genes that are not classified as informational and among the informational genes themselves, there are still large differences in the rates that these genes are inserted and deleted.ConclusionWhile the difference in informational gene rates contributes to rate variation, it is only a small fraction of the variation present; instead, a substantial amount of rate variation for insertions/deletions remains among both informational genes and among non-informational genes.

Dataset Information

Lateral gene transfer and gene duplication played a key role in the evolution of Mastigamoeba balamuthi hydrogenosomes.

Publications

Lateral gene transfer and gene duplication played a key role in the evolution of Mastigamoeba balamuthi hydrogenosomes.

Similar Datasets

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