Host-parasite interactions of an avian blood parasite elucidated by single-cell transcriptomics

Rapp, Tim Maximilian; Lautwein, Tobias; Peuß, Robert; Kurtz, Joachim; Krüger, Oliver; Chakarov, Nayden

Abstract

To date, the intricate cellular and molecular interplay between hosts and parasites is well described for a limited number of model systems. Recent methodological advances now allow deep insights in non-model symbioses, including such that ultimately appear barely antagonistic and may entail intense reciprocal manipulations. We applied single cell RNA-sequencing to blood samples of a wild, long-lived avian host, the Common Buzzard (Buteo buteo), infected with the malaria-like parasite Leucocytozoon toddi. We identified host cell types and their respective molecular toolkits involved in both, host immunity and parasite virulence. Comparing blood cell-type specific transcriptomic profiles between Buzzards with low and high parasitaemia, we gain insights into the parasitic immune evasion and potential modulation of the host immune response. The response of immune cells was overall low indicating immunosuppression under high parasitaemia, despite the reportedly low pathogenicity of the parasite, likely a result of long-lasting coevolution. Our study illuminates in rare detail a benign host-parasite interaction and bridges a large phylogenetic and symbiotic gap in the evolutionary gradient from parasitism to mutualism. The cell-type specific markers which we identify allow a more complete understanding of the evolutionary forces shaping host immunity.