Phylogenomics from transcriptomic "bycatch" clarify the origins and diversity of avian trypanosomes in North America.

Spencer C Galen,Janus Borner,Jason D Weckstein,Susan L Perkins,Tzen-Yuh Chiang

doi:10.1371/journal.pone.0240062

Abstract

The eukaryotic blood parasite genus Trypanosoma includes several important pathogens of humans and livestock, but has been understudied in wildlife broadly. The trypanosomes that infect birds are in particular need of increased attention, as these parasites are abundant and globally distributed, yet few studies have addressed their evolutionary origins and diversity using modern molecular and analytical approaches. Of specific interest are the deep evolutionary relationships of the avian trypanosomes relative to the trypanosome species that are pathogenic in humans, as well as their species level diversity in regions where they have been understudied such as North America. Here, we address these unresolved areas of study using phylogenomic data for two species of avian trypanosomes that were isolated as "bycatch" from host transcriptome assemblies, as well as a large 18S DNA barcode sequence dataset that includes 143 novel avian Trypanosoma 18S sequences from North America. Using a phylogenomic approach, we find that the avian trypanosomes are nested within a clade of primarily mammalian trypanosomes that includes the human pathogen Trypanosoma cruzi, and are paraphyletic with respect to the ruminant trypanosome Trypanosoma theileri. DNA barcode sequences showed that T. avium and an unidentified small, non-striated trypanosome that was morphologically similar to T. everetti are each represented by highly abundant and divergent 18S haplotypes in North America. Community-level sampling revealed that additional species-level Trypanosoma lineages exist in this region. We compared the newly sequenced DNA barcodes from North America to a global database, and found that avian Trypanosoma 18S haplotypes generally exhibited a marked lack of host specificity with at least one T. avium haplotype having an intercontinental distribution. This highly abundant T. avium haplotype appears to have a remarkably high dispersal ability and cosmopolitan capacity to evade avian host immune defenses, which warrant further study.

Highlights

Eukaryotic parasites are highly abundant, globally distributed, and of great concern for the health of humans, livestock, and wildlife
B) TCS haplotype network for North American avian trypanosomes with species delimitations depicted
By bioinformatically searching avian blood transcriptomes for parasite ‘bycatch’ and extracting Trypanosoma contigs from infected samples, we present here the first phylogenomic hypothesis for the relationships of avian trypanosome species within the broader phylogeny of Trypanosoma

Summary

Introduction

Eukaryotic parasites are highly abundant, globally distributed, and of great concern for the health of humans, livestock, and wildlife. The majority of eukaryotic parasite biodiversity is poorly known relative to the few species that have become model systems of disease. The development of powerful methods for generating DNA sequence data from non-model parasite groups for which genetic resources are scarce has created a window into the ecology and evolution of many poorly studied parasite lineages. In addition to the well-studied species that cause disease in humans and livestock, the genus Trypanosoma contains a diverse suite of species that are blood parasites of wildlife including mammals, birds, reptiles, amphibians, and fish, and infect a diversity of invertebrates that act as vectors between vertebrate hosts [7, 10,11,12,13]

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