Chromosome-level genome assembly of trypanosomatid parasite Lotmaria passim links chromosome duplication and divergence with infection of honey bees

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 novel 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 high synteny with assemblies of other trypanosomatids and especially closely related Leptomonas pyrrhocoris relatives. 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 tothis chromosome’s role in Leishmania infection of mammals and linking chromosome-level changes with adaptation to new hosts.