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

Abstract

Parasites and hosts perform fine-tuned cellular and molecular interactions, known from few well-explored model systems. Recent methodological advances now allow such deep insights into non-model parasites, their hosts, and their intense reciprocal manipulation. We applied single cell RNA-sequencing to blood samples of a long-lived bird host, infected at high and low intensity with malaria-related parasites. We identify diverse parasitic traits for immune evasion and potential manipulation of the avian host immune response. The transcriptomic response of immune cells was decoupled from the infection load, consistent with evidently low pathogenicity. Changes of immune cell populations showed low activation of adaptive immunity, such as clonal expansion of lymphoid cells. This absence of antagonism indicates immunosuppression by the parasite, which may mitigate virulence and thereby facilitate host-parasite coadaptation. The identified cell-type specific markers provide an important reference and will help to understand the evolutionary forces that shape host immunity in birds. Our study illuminates in rare molecular detail a benign host-parasite interaction and bridges a large coevolutionary knowledge gap of the gradient from parasitism to commensalism and mutualism.