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The Genome of Haemoproteus Tartakovskyi and Its Relationship To GBE TheGenomeofHaemoproteus tartakovskyi and Its Relationship to Human Malaria Parasites Staffan Bensch1,*,Bjo¨ rn Canba¨ck1, Jeremy D. DeBarry2, Tomas Johansson1, Olof Hellgren1, Jessica C. Kissinger2,3, Vaidas Palinauskas4, Elin Videvall1, and Gediminas Valkiu¯ nas4 1Department of Biology, Lund University, Sweden 2The Center for Tropical and Emerging Global Diseases, Athens, Georgia, USA 3Department of Genetics and Institute of Bioinformatics, University of Georgia Downloaded from https://academic.oup.com/gbe/article/8/5/1361/2939581 by guest on 02 October 2021 4Nature Research Centre, Vilnius, Lithuania *Corresponding author: E-mail: [email protected]. Data deposition: Haemoproteus tartakovskyi: The Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession LSRZ00000000. The version described in this paper is version LSRZ01000000. The genome assembly with predicted genes are available for download at http://mbio-serv2.mbioekol.lu.se/Malavi/Downloads. Plasmodium ashfordi: This project has been deposited at: the NCBI Sequence Read Archive under the accession number PRJNA311546. The assembled transcripts are available for download at http://mbio-serv2.mbioekol.lu.se/Malavi/Downloads. Accepted: April 4, 2016 Abstract The phylogenetic relationships among hemosporidian parasites, including the origin of Plasmodium falciparum,themostvirulent malaria parasite of humans, have been heavily debated for decades. Studies based on multiple-gene sequences have helped settle many of these controversial phylogenetic issues. However, denser taxon sampling and genome-wide analyses are needed to con- fidently resolve the evolutionay relationships among hemosporidian parasites. Genome sequences of several Plasmodium parasites are available but only for species infecting primates and rodents. To root the phylogenetic tree of Plasmodium, genomic data from related parasites of birds or reptiles are required. Here, we use a novel approach to isolate parasite DNA from microgametes and describe the first genome of a bird parasite in the sister genus to Plasmodium, Haemoproteus tartakovskyi. Similar to Plasmodium parasites, H. tartakovskyi has a small genome (23.2 Mb, 5,990 genes) and a GC content (25.4%) closer to P. falciparum (19.3%) than to Plasmodium vivax (42.3%). Combined with novel transcriptome sequences of the bird parasite Plasmodium ashfordi, our phylo- genomic analyses of 1,302 orthologous genes demonstrate that mammalian-infecting malaria parasites are monophyletic, thus rejecting the repeatedly proposed hypothesis that the ancestor of Laverania parasites originated from a secondary host shift from birds to humans. Genes and genomic features previously found to be shared between P. falciparum and bird malaria parasites, but absent in other mammal malaria parasites, are therefore signatures of maintained ancestral states. We foresee that the genome of H. tartakovskyi will open new directions for comparative evolutionary analyses of malarial adaptive traits. Key words: apicomplexa, haemoproteus, host switching, phylogenomics, Plasmodium, Plasmodium ashfordi, transcriptome. Introduction contain over 150 described species infecting mammals, birds, One hundred years ago, species in the genus Haemoproteus and reptiles within the mainly parasitic phylum Apicomplexa and related avian hemosporidians were essential model or- (Chromalveolata) (Perkins 2014). Closely related to ganisms for uncovering the complex life cycle of malaria par- Plasmodium are several genera of other hemosporidian para- asites (Martinsen and Perkins 2013), including the discoveries sites infecting mammals (Hepatocystis, Nycteria,and of exflagellation (MacCallum 1897), sporogony in mosquitoes Polychromophilus), birds (Haemoproteus, Leucocytozoon, (Ross 1898), and tissue merogony (Aragao 1908). These im- and Garnia), and reptiles (Saurocytozoon, Fallisia, Garnia, portant life stages forgo the asexual replication in erythrocytes and Haemocystidium)(Valkiu¯ nas 2005; Perkins 2014). To that is associated with malaria. Malaria parasites (Plasmodium) date, there is no consensus on the phylogenetic relationship ß The Author 2016. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Genome Biol. Evol. 8(5):1361–1373. doi:10.1093/gbe/evw081 Advance Access publication April 13, 2016 1361 Bensch et al. GBE between hemosporidian parasites. Conflicting phylogenetic sequences of multiple genes from a parasite (outgroup) hypotheses result from 1) heterogeneous data sets with re- unquestioned as being more distantly related to all the spect to the genes investigated, limited taxon sampling, and Plasmodium species than those ingroup taxa are to each choice of outgroups and 2) saturation of phylogenetic signals other, but yet not so distantly related that sequence align- that is further complicated by drastically variable GC contents ments become problematic. of the parasite genomes (Da´valos and Perkins 2008; Martinsen A potentially useful outgroup to resolve the phylogenetic and Perkins 2013; Perkins 2014). As a consequence, it is chal- relationships within Plasmodium could be any species of lenging to reach unambiguous understanding of the evolu- hemosporidian parasites in the genus Haemoproteus.There tionary history of genes, metabolic pathways, and adaptive are about 150 Haemoproteus parasites described (Valkiu¯ nas traits within this important group of parasites. 2005), but the genus may contain 10-fold more (cryptic) spe- The evolutionary origin of the most virulent malaria parasite cies as inferred from the high diversity of cytochrome b hap- Downloaded from https://academic.oup.com/gbe/article/8/5/1361/2939581 by guest on 02 October 2021 of humans, Plasmodium falciparum, has been debated for lotypes (Outlaw and Ricklefs 2014). Similar to Plasmodium decades (Hagner et al. 2007). Most of the more recent studies parasites, Haemoproteus spp. produce malarial pigment have found it to be closely related to the other mammalian (hemozoin) in blood cells and their sexual reproduction takes malaria parasites (fig. 1A and B)(Perkins and Schall 2002; place in dipteran vectors after ingestion of a blood meal. The Martinsen et al. 2008; Outlaw and Ricklefs 2011; Silva et al. diploid stage of the parasite is then followed by a series of life 2011; Schaer et al. 2013; Borner et al. 2016)incontrastto stages that eventually result in (haploid) infectious sporozoites several studies from the 1990s that proposed an origin from a that migrate to the salivary gland of the vector and subse- Plasmodium parasite of birds shifting hosts to mammals (fig. quently will be transmitted to a vertebrate host during the 1C and D)(Waters et al. 1991; Escalante et al. 1998; next blood meal. The main vectors of Plasmodium parasites McCutchan et al. 1996). However, more recent studies are various species of blood-sucking mosquitoes (Culicidae), based on genomic data have also found support for a rela- whereas Haemoproteus parasites are vectored by biting tionship between P. falciparum and bird Plasmodium (Pick midges (Ceratopogonidae; parasites of the subgenus et al. 2011). It is now well established that P. falciparum is Parahaemoproteus) and louse flies (Hippoboscidae; parasites one of many closely related species in the subgenus Laverania of the subgenus Haemoproteus)(Valkiu¯ nas 2005). Another that infects gorillas and chimpanzees (Prugnolle et al. 2010) important difference to Plasmodium is that Haemoproteus and that P. falciparum most likely originated from a parasite of parasites do not use host red blood cells for asexual replica- gorillas (Liu et al. 2010). Yet, these important findings of the tion, only the gametocytes can be found in the blood; instead, recent evolutionary history of P. falciparum (Keeling and the replication takes place in various internal organs of the Rayner 2015) do not answer the question of whether the host. ancestor of extant Laverania comes from Plasmodium para- Using Haemoproteus parasites as outgroups in phyloge- sites of birds or mammals. Resolving this question will require netic analyses of Plasmodium parasites is, however, not Haemoproteus ACPlasmodium “Laverania” Plasmodium “birds” Plasmodium “birds” Plasmodium “Laverania” Haemoproteus Plasmodium “mammals” Plasmodium “mammals” BDHaemoproteus Haemoproteus Plasmodium “birds” Plasmodium “mammals” Plasmodium “Laverania” Plasmodium “birds” Plasmodium “mammals” Plasmodium “Laverania” FIG.1.—Four phylogenetic hypotheses (A–D) illustrating the proposed relationships between species of Haemoproteus, Plasmodium of birds (including reptiles), Plasmodium of mammals, and Plasmodium of the subgenus Laverania, which contains the human parasite Plasmodium falciparum. Bird (and reptile) parasite branches are labeled in blue and mammal parasite branches in green. Triangular branch tips contain multiple species (in the range of 100–1,000); the Laverania branch may include about ten species infecting apes. Data presented in this work support phylogenetic hypothesis A. 1362 Genome Biol. Evol. 8(5):1361–1373. doi:10.1093/gbe/evw081 Advance Access publication April 13, 2016 Genome of H. tartakovskyi GBE straightforward
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