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Complex patterns of gene fission in the eukaryotic folate biosynthesis pathway - PubMed

  • ️Wed Jan 01 2014

Complex patterns of gene fission in the eukaryotic folate biosynthesis pathway

Finlay Maguire et al. Genome Biol Evol. 2014.

Abstract

Shared derived genomic characters can be useful for polarizing phylogenetic relationships, for example, gene fusions have been used to identify deep-branching relationships in the eukaryotes. Here, we report the evolutionary analysis of a three-gene fusion of folB, folK, and folP, which encode enzymes that catalyze consecutive steps in de novo folate biosynthesis. The folK-folP fusion was found across the eukaryotes and a sparse collection of prokaryotes. This suggests an ancient derivation with a number of gene losses in the eukaryotes potentially as a consequence of adaptation to heterotrophic lifestyles. In contrast, the folB-folK-folP gene is specific to a mosaic collection of Amorphea taxa (a group encompassing: Amoebozoa, Apusomonadida, Breviatea, and Opisthokonta). Next, we investigated the stability of this character. We identified numerous gene losses and a total of nine gene fission events, either by break up of an open reading frame (four events identified) or loss of a component domain (five events identified). This indicates that this three gene fusion is highly labile. These data are consistent with a growing body of data indicating gene fission events occur at high relative rates. Accounting for these sources of homoplasy, our data suggest that the folB-folK-folP gene fusion was present in the last common ancestor of Amoebozoa and Opisthokonta but absent in the Metazoa including the human genome. Comparative genomic data of these genes provides an important resource for designing therapeutic strategies targeting the de novo folate biosynthesis pathway of a variety of eukaryotic pathogens such as Acanthamoeba castellanii.

Keywords: Diaphoretickes; comparative genomics; phylogenetics; pterin biosynthesis.

© The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

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Figures

F<sc>ig</sc>. 1.—
Fig. 1.—

Part of the folate biosynthesis pathway with intermediate chemical states of the pathway illustrated. Protein and gene names that encode each step of the pathway are given.

F<sc>ig</sc>. 2.—
Fig. 2.—

Presence, absence, and fusion state of putative folate pathway encoding genes across the eukaryotes. Taxonomic distribution of the pterin branch of the folate biosynthesis pathway. The red boxes and connecting lines indicate a gene fusion, black boxes represents presence of a putative homologue, and gray indicates gene not identified in the genome sequence data. Amoebozoa and Opisthokonta were formerly referred to as the “unikonts,” and likewise SAR, Excavata, and Archaeplastida were formerly referred to as the “bikonts.” Note that the putative folB of Trichoplax adhaerens and the putative folB-folK fusion of Nematostella vectensis were removed from phylogenetic analyses due to poor alignment of these sequences, as such their provenance and evolutionary ancestry remains questionable and are therefore indicated by a question mark at the relevant position.

F<sc>ig</sc>. 3.—
Fig. 3.—

Phylogeny of the Apusomonadida, Breviata, Opisthokonta, and Amoebozoa demonstrating variation in the folB-folK-folP fusion gene. Tree topology was calculated using a concatenated alignment of conserved genes identified in (Torruella et al. 2012) and represents the best-known likelihood tree from 100 ML searches in RAxML (PROTCAT+LG) with 1,000 nonrapid bootstraps. ML-BS is an abbreviation of maximum likelihood bootstrap values, FolB-folK-folP fusion gene domain architecture of taxa included is listed down the right column, and fusion state is denoted by the presence/absence of connecting lines. Inferred gene/domain losses are shown as shadow domains. See key for guide to tree topology support values and character state changes. Domain duplication is indicated as (D) in a box of the appropriate domain colour, fission by domain loss events are denoted as (FL5–9) and specific fission events as (F1–4). Total losses of complete ORFs are not illustrated. Note that the putative folB of Trichoplax adhaerens and the putative folB-folK fusion of Nematostella vectensis were removed from phylogenetic analyses due to poor alignment of these sequences, as such their provenance and evolutionary ancestry remains questionable and are therefore indicated by a question mark at the relevant position.

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