Somy evolution in the honey bee infecting trypanosomatid parasite Lotmaria passim

Authors: MARKOWITZ, LINDSEY - University Of Maryland; NEARMAN, ANTHONY - University Of Maryland; ZEXUAN, ZHAO - University Of Maryland; Boncristiani, Dawn; BUTENKO, ANZHELIKA - University Of Ostrava; DE PABLOS, LUIS MIGUEL - University De Granada; MACHADO, CARLOS A. - University Of Maryland; SCHWARZ, RYAN S. - Fort Lewis College; PALMER-YOUNG, EVAN C. - Orise Fellow; Evans, Jay

Submitted to: G3: Genes, Genomes, Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2024
Publication Date: 6/17/2025
Citation: Markowitz, L., Nearman, A., Zexuan, Z., Boncristiani, D.L., Butenko, A., De Pablos, L., Machado, C., Schwarz, R., Palmer-Young, E., Evans, J.D. 2025. Somy evolution in the honey bee infecting trypanosomatid parasite Lotmaria passim. G3: Genes, genomics, genetics. 15. Article 258. https://doi.org/10.1093/g3journal/jkae258.
DOI: https://doi.org/10.1093/g3journal/jkae258

Interpretive Summary: Honey bees are critical for agriculture yet they face an uncertain future in the face of numerous diseases. Lotmaria is a gut parasite that has been linked to colony losses. There are no registered treatments for this parasite and little is known about its biology. The genome features described here help show how this parasite is related to known parasites that have received much study as medical diseases. We described ways that genome data can be used to identify key interactions with bee hosts and researchers and industry members might use these insights to combat a little-known but worldwide bee parasite. Newly developed treatments for this parasite would help stabilize bee populations and lead to lower pollination costs.

Technical Abstract: Lotmaria passim is a ubiquitous trypanosomatid parasite of honey bees nestled within the medically important subfamily Leishmaniinae. Although this parasite is associated with honey bee colony losses, the original draft genome—which was completed before its differentiation from the closely related Crithidia mellificae—has remained the reference for this species despite lacking improvements from newer methodologies. Here, we report the updated sequencing, assembly, and annotation of the BRL-type (Bee Research Laboratory) strain (ATCC PRA-422) of Lotmaria passim. The nuclear genome assembly has been resolved into 31 complete chromosomes and is paired with an assembled kinetoplast genome consisting of a maxicircle and 30 minicircle sequences. The assembly spans 33.7 Mb and contains very little repetitive content, from which our annotation of both the nuclear assembly and kinetoplast predicted 10,288 protein-coding genes. Analyses of the assembly revealed evidence of a recent chromosomal duplication event within chromosomes 5 and 6 and provided evidence for a high level of aneuploidy in this species, mirroring the genomic flexibility employed by other trypanosomatids as a means of adaptation to different environments. This high-quality reference can therefore provide insights into adaptations of trypanosomatids to the thermally regulated, acidic, and phytochemically rich honey bee hindgut niche, which offers parallels to the challenges faced by other Leishmaniinae during the challenges they undergo within insect vectors, during infection of mammals, and exposure to antiparasitic drugs throughout their multi-host life cycles. This reference will also facilitate investigations of strain-specific genomic polymorphisms, their role in pathogenicity, and the development of treatments for pollinator infection.