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. 2014 Jun 19;10(7):689-701.
doi: 10.7150/ijbs.8327. eCollection 2014.

Amoebozoa possess lineage-specific globin gene repertoires gained by individual horizontal gene transfers

Jasmin Dröge  1 , Dorota Buczek  2 , Yutaka Suzuki  3 , Wojciech Makałowski  4
Affiliations

Amoebozoa possess lineage-specific globin gene repertoires gained by individual horizontal gene transfers

Jasmin Dröge et al. Int J Biol Sci. .

Abstract

The Amoebozoa represent a clade of unicellular amoeboid organisms that display a wide variety of lifestyles, including free-living and parasitic species. For example, the social amoeba Dictyostelium discoideum has the ability to aggregate into a multicellular fruiting body upon starvation, while the pathogenic amoeba Entamoeba histolytica is a parasite of humans. Globins are small heme proteins that are present in almost all extant organisms. Although several genomes of amoebozoan species have been sequenced, little is known about the phyletic distribution of globin genes within this phylum. Only two flavohemoglobins (FHbs) of D. discoideum have been reported and characterized previously while the genomes of Entamoeba species are apparently devoid of globin genes. We investigated eleven amoebozoan species for the presence of globin genes by genomic and phylogenetic in silico analyses. Additional FHb genes were identified in the genomes of four social amoebas and the true slime mold Physarum polycephalum. Moreover, a single-domain globin (SDFgb) of Hartmannella vermiformis, as well as two truncated hemoglobins (trHbs) of Acanthamoeba castellanii were identified. Phylogenetic evidence suggests that these globin genes were independently acquired via horizontal gene transfer from some ancestral bacteria. Furthermore, the phylogenetic tree of amoebozoan FHbs indicates that they do not share a common ancestry and that a transfer of FHbs from bacteria to amoeba occurred multiple times.

Keywords: Amoebozoa; globin genes.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interest exists.

Figures

Figure 1
Figure 1
Comparison of the genomic neighborhood of the FHb genes from D. discoideum and D. purpureum. The direct neighboring genes of the FHbA and FHbB genes of D. discoideum and D. purpureum are shown. The directions of the boxes indicate the genomic orientations of the genes, i.e. a box directed to the right equates the plus strand, directed to the left equates the minus strand. Boxes with the same color represent orthologs, while grey boxes indicate that those genes do not possess an ortholog in this genomic location. For each gene either the gene symbol or the accession number provided by dictyBase is given. The FHbs of D. discoideum are located on chromosome 6 in a head-to-tail orientation. In contrast, the FHbs of D. purpureum are lying on two different scaffolds. The FHbA genes of the two amoebas lie in a short conserved syntenic block.
Figure 2
Figure 2
Alignment of amoebozoan FHbs to the Hmp protein of Escherichia coli. The alignment was created with MUSCLE. Conserved residues are shaded in different levels of grey. Residues that are conserved in all sequences are in dark grey. The secondary structure of the Hmp protein is given above the alignment (PDB: 1gvh). Predicted α-helices and β-strands are indicated as red and yellow lines, respectively, below the corresponding sequences. The positions of the introns are marked with green boxes and by arrows below the alignment. The topological positions of the introns as compared to sperm whale Mb are indicated below the alignment. The helix structure of the sperm whale myoglobin was superimposed on the alignment and indicated by violet bars above the alignment.
Figure 3
Figure 3
Radial maximum likelihood tree of FHb proteins. The colors of branches correspond to the taxonomic classification of the used sequences. Bootstrap support (bs) and posterior probability (pp) values equal or greater than 50 % are given (bs/pp). The FHb proteins cluster in four highly supported clades (1-4). For a description of used abbreviations please refer to Supplementary Material: table S1.
Figure 4
Figure 4
Alignment of the trHbs of A. castellanii to trHbN of Tetrahymena pyriformis and trHbO of Thermobifida fusca. The alignment was created with MUSCLE. Conserved residues are shaded in different levels of grey. Residues that are conserved in all sequences are in dark grey. The secondary structure of the trHb proteins of T. pyriformis (PDB: 3aq9) and T. fusca (PDB: 2bmm) are given. Predicted α-helices are indicated as red lines, below the corresponding sequences. The positions of the introns are marked with green boxes and by arrows below the alignment. The topological positions of the introns as compared to sperm whale Mb are indicated below the alignment. The helix structure of the sperm whale myoglobin was superimposed on the alignment and indicated by violet bars above the alignment.
Figure 5
Figure 5
Radial maximum likelihood tree of trHb proteins. The colors of branches correspond to the taxonomic classification of the used sequences. Bootstrap support (bs) and posterior probability (pp) values equal or greater than 50 % are given (bs/pp). The trHb proteins cluster in three highly supported clades (I-III), in accordance to their classification. For a description of used abbreviations please refer to Supplementary Material: table S1.
Figure 6
Figure 6
Radial maximum likelihood tree of single-domain globins and the SDFgb of H. vermiformis. The colors of branches correspond to the taxonomic classification of the used sequences. Bootstrap support (bs) and posterior probability (pp) values equal or greater than 50 % are indicated (bs/pp). The SDFgb of H. vermiformis (HaveSDFgb) clusters with two bacterial SDFgbs. For a description of used abbreviations please refer to Supplementary Material: table S1.
Figure 7
Figure 7
Phylegenetic relationships between studied Amoebozoa organisms. The tree is based on Adl et al. Please note that branch length is not to scale. Type of globin found in a given group is indicated in dark blue inside the group circles.
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