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Amoebozoa Possess Lineage-Specific Globin Gene Repertoires Gained by Individual Horizontal Gene Transfers

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Amoebozoa Possess Lineage-Specific Globin Gene Repertoires Gained by Individual Horizontal Gene Transfers Int. J. Biol. Sci. 2014, Vol. 10 689 Ivyspring International Publisher International Journal of Biological Sciences 2014; 10(7): 689-701. doi: 10.7150/ijbs.8327 Research Paper Amoebozoa Possess Lineage-Specific Globin Gene Repertoires Gained by Individual Horizontal Gene Transfers Jasmin Dröge1, Dorota Buczek1,2, Yutaka Suzuki3, and Wojciech Makałowski1,3 1. Institute of Bioinformatics, Faculty of Medicine, University of Muenster, Niels Stensen Str. 14, 48149 Muenster, Germany 2. Institute of Molecular Biology and Biotechnology, A. Mickiewicz University, Poznan, Poland 3. Department of Medical Genomic Sciences, University of Tokyo, Tokyo, Japan Corresponding author: [email protected] © Ivyspring International Publisher. This is an open-access article distributed under the terms of the Creative Commons License (http://creativecommons.org/ licenses/by-nc-nd/3.0/). Reproduction is permitted for personal, noncommercial use, provided that the article is in whole, unmodified, and properly cited. Received: 2013.12.10; Accepted: 2014.03.24; Published: 2014.06.19 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 phy- logenetic 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 Acan- thamoeba 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. Key words: Amoebozoa, globin genes Introduction Globins (Gbs) are small heme proteins that have through H [8]. In contrast, the members of the T line- been found in all kingdoms of life in a wide range of age exhibit a 2/2 structure characterized by a short- different species [1-3]. Gbs are able to bind various ened or completely deleted A helix, a missing D helix, gaseous ligands, such as oxygen and nitric oxide, and and the substitution of the proximal F helix by a pol- have diverse functions, e.g. in respiration and nitric ypeptide segment [9]. The F globin family consists of oxide detoxification [4]. The globin superfamily can flavohemoglobins (FHbs), FHb-like globins with N- be divided into three lineages, namely the S, F, and T and C-terminal extensions, and related single-domain globins, which belong to two structural classes [5-7]. globins (SDFgbs). The chimeric FHb proteins possess The members of the F and S lineages possess the typ- an N-terminal globin domain and a C-terminal FAD- ical globin fold, i.e. a 3-over-3 (3/3) α-helical fold and NAD(P)H-binding reductase domain. Increasing consisting of seven or eight α-helices, designated A evidence indicates that FHbs protect bacteria and http://www.ijbs.com Int. J. Biol. Sci. 2014, Vol. 10 690 simple eukaryotes, including yeast, against the toxic liver abscess [32]. Likewise, also some members of the effects of nitric oxide likely via the nitroxylation of genus Acanthamoeba have been identified as origin of oxygen [10-13]. The S globin family comprises chi- amebic infections in humans [33]. meric globin-coupled sensors (GCSs), protoglobins The presented study aims to define the globin (Pgbs), and related single-domain globins (SDSgbs). gene repertoire of amoebozoan species. Eleven dif- The GCSs can be further categorized as either aero- ferent species of the subphyla Conosa (infraphyla tactic or gene regulating [14]. The globins of the T Mycetozoa, Archamoebae) and Lobosa (infraphyla lineage were named truncated hemoglobins (trHbs) Tubulinea, Acanthopodina) were scanned for the because of their shortened primary structure. Based presence of globin genes. We show that the examined on phylogenetic analyses and structural differences Amoebozoa possess lineage-specific globin gene rep- the trHbs can be further divided into three groups, i.e. ertoires, composed of either FHbs, SDFgbs, or trHbs group I (trHbN), II (trHbO), and III (trHbP) [15, 16]. that have been likely gained through multiple hori- Several distinct functions for the trHbs have been zontal gene transfer events from ancestral bacteria. proposed, including nitric oxide detoxification, oxy- gen/nitric oxide sensing, ligand/substrate storage, Methods etc. [15, 17]. Identification of amoebozoan globin genes A model of globin evolution has been suggested in which the three lineages descent from a single Initially, the two previously described FHbs of common ancestor that likely resembled an extant D. discoideum [34] were used to search the SDFgb [3, 7]. It is assumed that globins emerged only non-redundant protein database of NCBI for homol- in bacteria [7]. Later, the eukaryote and archaeal 3/3 ogous amoebozoan globin proteins employing the and 2/2 globin genes originated from horizontal gene BLASTp algorithm with default parameters [35]. The transfers (HGT) of bacterial SDFgb and trHb genes, retrieved sequences and the globin sequences of two respectively [5-7]. This is supported by several studies fungi, Schizophyllum commune and Saccharomyces cere- that demonstrate that HGT events shaped the phyletic visiae, were used to search the genomes of A. castel- distribution of globin genes in plants, fungi, and uni- lanii, D. discoideum, D. fasciculatum, D. purpureum, E. cellular eukaryotes [3, 5, 6, 16, 18-24]. Finally, it is dispar, E. histolytica, E. invadens, E. moshkovskii, P. pol- known that HGT events played a major role in the ycephalum and Polysphondylium pallidum for the pres- evolution of various species [25, 26]. ence of additional globin genes. This was done by a Although the evolution of globins has been in- tBLASTn search applying varying parameters: tensively studied in several species from all kingdoms e-value 0.1, 0.001, matrix: BLOSUM62, BLOSUM45, of life, only little is known about their origins and soft masking of query sequence. Likewise, a tBLASTn distribution in unicellular eukaryotes, such as the search was conducted against TBestDB [36]. Addi- Amoebozoa [27]. The Amoebozoa are a phylum of tionally, the transcriptome of A. castellanii was ana- amoeboid protozoa that move by the means of pseu- lyzed for the presence of globin sequences (Buczek et dopodia. They are closely related to Opisthokonts al., unpublished data). Subsequently, the similarity (Metazoa/fungi group) and can be divided into six search was repeated with the newly found sequences. monophyletic clades within two main groups, the The intron/exon structures of the novel genes were Lobosea and the Conosea [28, 29]. They adopted dif- manually annotated, guided by tBLASTn results, ferent habitats and life styles, such as free-living uni- GENSCAN [37], and NetGene2 predictions [38, 39]. cellular amoeba, obligate parasitic amoeba, social Intron positions with respect to the coding sequences amoeba, and true slime molds. The free-living were reported with reference to the secondary struc- Amoebozoa are common inhabitants of soils and wa- ture of the protein. This was done by aligning the ter, where they represent one of the main predators of amoebozoan globin proteins to myoglobin of the bacteria [30]. Acanthamoeba castellanii is the most fre- sperm whale (UniProtKB: P02185.2). FUGUE [40] and quently found amoeba in soil and plays an important SMART [41] were used to validate the annotated se- role in a variety of environments. One of the quences as globin genes. A table of sequences used in best-known amoebas is the social amoeba Dictyoste- the subsequent analyses is provided in the supple- lium discoideum that has been studied for decades. D. mentary materials (Table S1). All genes used in the discoideum is a solitary amoeba that can achieve mul- consecutive analyses were labeled with first two let- ticellularity under starvation by aggregation and ters of the binary species name and a suffix in cases morphogenesis into a fruiting body [31]. Some multiple copies are present in a single genome. amoebas are known to cause infectious diseases in Shared synteny is a reliable criterion to prove humans, for instance the intestinal parasite Entamoeba orthology between genomic segments and to trace histolytica which can induce amebic colitis and amebic back the evolution of those segments. The neighbor- http://www.ijbs.com Int. J. Biol. Sci. 2014, Vol. 10 691 ing genes of the FHbs from the social amoebas D. dis- were removed from the data set, e.g. highly similar coideum, D. purpureum, D. fasciculatum, and P. pallidum globins from different subspecies. Based on ubiqui- were identified using the genome browser and the tous clustering with high statistical support and short tBLASTn tool provided by dictyBase [42, 43]. Orthol- branches, sequences with identity equal or higher ogous genes were defined as reciprocal best hits than 85 percent were considered as redundant and (RBHs) via tBLASTn and BLASTp searches. Addi- consequently only one from a given cluster was used tionally, the direct neighbors of the trHbs of A. castel- for the phylogenetic inference. lanii were determined via GENSCAN and subsequent Next, the sequences were divided into two data BLASTp searches. We did not conduct a synteny sets, one comprising FHbs (66 sequences), the other analysis of the FHb genes of P.
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