Single-cell RNA-seq profiling of individual Biomphalaria glabrata immune cells with a focus on immunologically relevant transcripts

Abstract

The immune cells of the snail Biomphalaria glabrata are classified into hyalinocyte and granulocyte subtypes. Both subtypes are essential for the proper functioning of the snail immune response, which we understand best within the context of how it responds to challenge with the human parasite Schistosoma mansoni. Granulocytes are adherent phagocytic cells that possess conspicuous granules within the cell cytoplasm. Hyalinocytes, on the other hand, are predominantly non-adherent and are known to produce a handful of anti-S. mansoni immune effectors. While our understanding of these cells has progressed, an in-depth comparison of the functional capabilities of each type of immune cell has yet to be undertaken. Here, we present the results of a single-cell RNA-seq study in which single granulocytes and hyalinocytes from S. mansoni-susceptible M-line B. glabrata and S. mansoni-resistant BS-90 B. glabrata are compared without immune stimulation. This transcriptomic analysis supports a role for the hyalinocytes as producers of immune effectors such as biomphalysin and thioester-containing proteins. It suggests that granulocytes are primarily responsible for producing fibrinogen-related proteins and are armed with various pattern-recognition receptors such as toll-like receptors with a confirmed role in the anti-S. mansoni immune response. This analysis also confirms that the granulocytes and hyalinocytes of BS-90 snails are generally more immunologically prepared than their M-line counterparts. As the first single-cell analysis of the transcriptional profiles of B. glabrata immune cells, this study provides crucial context for understanding the B. glabrata immune response. It sets the stage for future investigations into how each immune cell subtype differs in its response to various immunological threats.

Keywords: Biomphalaria glabrata; Fibrinogen-related proteins; Hemocyte; Pattern recognition receptor; Schistosoma mansoni; Single-cell RNA-seq.