BACKGROUND: The protist family Trypanosomatidae includes parasites of insects, vertebrates, plants, and even other unicellular eukaryotes. The genomes of these species harbor clues to the evolution of parasitism, adaptation to new hosts, and infection of mammals. We present an analysis of a chromosome-level genome assembly of Lotmaria passim, the most prevalent known trypanosomatid of honey bees, linking genome sequence and organization to gene expression and infection of bees. RESULTS: The genome showed a high degree of synteny with assemblies of other trypanosomatids and especially to the closely related Leptomonas pyrrhocoris. It included four copies of chromosomes that shared ancestry with the tetrasomic Leishmania Chromosome 31 and are consistently supernumerary throughout Trypanosomatidae. However, these chromosomes showed lower similarity to L. passim relatives than did the genome overall, with sufficient variation across haplotypes to distinguish two separate disomic chromosomes. Transcriptomic analyses showed that these chromosomes are enriched in genes upregulated during bee infection, and each include five paralogs of the GP63 gene implicated in infection of both insects and mammals. Patterns of expression in bees suggested decreased protein synthesis, a shift from carbohydrate- to amino acid-based metabolism, and reduced cell motility in bee guts versus cell culture. In contrast, genes involved in cell adhesion were upregulated, consistent with the importance of attachment to insect tissue in this species and the family overall. CONCLUSIONS: Our analysis links differentiation of a conserved supernumerary chromosome with infection of bees, parallel to this chromosome's role in Leishmania infection of mammals and linking chromosome-level changes with adaptation to new hosts.

Czech Academy of Sciences Institute of Parasitology České Budějovice 370 05 Czech Republic

Faculty of Science University of South Bohemia České Budějovice 370 05 Czech Republic

Life Science Research Centre Faculty of Science University of Ostrava Ostrava 710 00 Czech Republic

USDA ARS Bee Research Laboratory 10300 Baltimore Ave BARC East Bldg 306 Rm 313 Beltsville MD 20705 USA

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