Global Kinetoplastea phylogeny inferred from a large-scale multigene alignment including parasitic species for better understanding transitions from a free-living to a parasitic lifestyle

Abstract

All members of the order Trypanosomatida known to date are parasites that are most likely descendants of a free-living ancestor. Trypanosomatids are an excellent model to assess the transition from a free-living to a parasitic lifestyle, because a large amount of experimental data has been accumulated for well-studied members that are harmful to humans and livestock (Trypanosoma spp. and Leishmania spp.). However, recent advances in our understanding of the diversity of trypanosomatids and their close relatives (i.e., members of the class Kinetoplastea) have suggested that the change in lifestyle took place multiple times independently from that which gave rise to the extant trypanosomatid parasites. In the current study, transcriptomic data of two parasitic kinetoplastids belonging to orders other than Trypanosomatida, namely Azumiobodo hoyamushi (Neobodonida) and Trypanoplasma borreli (Parabodonida), were generated. We re-examined the transition from a free-living to a parasitic lifestyle in the evolution of kinetoplastids by combining (i) the relationship among the five orders in Kinetoplastea and (ii) that among free-living and parasitic species within the individual orders. The former relationship was inferred from a large-scale multigene alignment including the newly generated data from Azumiobodo and Trypanoplasma, as well as the data from another parasitic kinetoplastid, Perkinsela sp., deposited in GenBank; and the latter was inferred from a taxon-rich small subunit ribosomal DNA alignment. Finally, we discuss the potential value of parasitic kinetoplastids identified in Parabodonida and Neobodonida for studying the evolutionary process that turned a free-living species into a parasite.

Evolution of metabolic capabilities and molecular features of diplonemids, kinetoplastids, and euglenids

“…The assembled transcriptomes of Neobodo designis (Kinetoplastea, Neobodonida) and Eutreptiella gymnastica (Euglenida) were downloaded from the Marine Microbial Eukaryote Transcriptome Sequencing Project database (MMETSP) [11]. We used the transcriptome assembly of Euglena gracilis strain Z generated by Ebenezer et al and that of Azumiobodo hoyamushi generated by Yazaki and colleagues [15,180]. Redundant transcripts were filtered out from all the transcriptome assemblies using the CD-HIT-EST software v.4.6.7 [181] with the sequence identity threshold of 90%.…”

Neobodonids are dominant kinetoplastids in the global ocean

“…An analysis of abundant OTUs revealed such associations for three neobodonid OTUs. The only parasitic neobodonid described so far is Azumiobodo (Hirose et al ., ; Kumagai et al ., ; Yazaki et al ., ), which was poorly represented within our samples (about 7 000 reads in total). Significantly more abundant were the novel parasite candidates: OTUs #4802, #3742, and #2083 (with 15 000, 29 000 and 45 000 reads, respectively).…”

“…However, the bulk of bodonids described so far belong to the clade Metakinetoplastina, which also includes the crown group of trypanosomatids (Moreira et al, 2004). Within Metakinetoplastina, three lineages termed Eu-, Neo-and Parabodonida are recognized (Luke s et al, 2014;Yazaki et al, 2017). These bodonid lineages harbour mostly freeliving bacteriovores from aquatic environments and soil, where they usually constitute a relatively minor group of uncertain ecological significance (Atkins et al, 2000;Glaser et al, 2014;L opez-García et al, 2003).…”

Evolution of protein trafficking in kinetoplastid parasites: Complexity and pathogenesis

“…With numerous lineage‐specific features (Figure A), they are among the most divergent taxa from their animal and plant hosts . Significantly, most known kinetoplastids are parasitic, and it is likely that parasitism evolved within Euglenozoa more than once as a result of adaptation . The most familiar examples are the trypanosomes and Leishmania in the order Trypanosomatida.…”