Extracellular vesicle signatures and protein citrullination are modified in shore crabs ( Carcinus maenas ) infected with Hematodinium sp

Abstract

Epizootiologists recurrently encounter symbionts and pathobionts in the haemolymph (blood equivalent) of shellfish. One such group is the dinoflagellate genus Hematodinium , which contains several species that cause debilitating disease in decapod crustaceans. The shore crab Carcinus maenas acts as a mobile reservoir of microparasites, including Hematodinium sp., thereby posing a risk to other co-located commercially important species, e.g. velvet crabs ( Necora puber ). Despite the widespread prevalence and documented seasonality of Hematodinium infection dynamics, there is a knowledge gap regarding host-pathogen antibiosis, namely, how Hematodinium avoids the host’s immune defences. Herein, we interrogated the haemolymph of Hematodinium -positive and Hematodinium -negative crabs for extracellular vesicle (EV) profiles (a proxy for cellular communication), alongside proteomic signatures for post-translational citrullination/deimination performed by arginine deiminases, which can infer a pathologic state. Circulating EV numbers in parasitized crab haemolymph were reduced significantly, accompanied by smaller EV modal size profiles (albeit non-significantly) when compared to Hematodinium -negative controls. Differences were observed for citrullinated/deiminated target proteins in the haemolymph between the parasitized and control crabs, with fewer hits identified overall in the former. Three deiminated proteins specific to parasitized crab haemolymph were actin, Down syndrome cell adhesion molecule (DSCAM), and nitric oxide synthase – factors that contribute to innate immunity. We report, for the first time, Hematodinium sp. could interfere with EV biogenesis, and that protein deimination is a putative mechanism of immune-modulation in crustacean- Hematodinium interactions.

Infection of Norway lobster ( Nephrops norvegicus ) by the parasite Hematodinium sp.: insights from 30 years of field observations

“…Recent evidence from a shore crab– Hematodinium pathosystem does not link Hematodinium sp. with gross immunosuppression of the host, but rather a lack of haemocyte reactivity to the parasite [ 11 , 21 ]. It is possible that humoral-mediated defence mechanisms might allow larger hosts (being more immune-competent than smaller conspecifics) to counteract Hematodinium sp.…”

“…Hematodinium sp. prevalence in Nephrops from the CSA has been studied since its apparent emergenceor at least, at a level that evoked comment from fishers-in the late 1980s, with estimates available from 1989 to 2008 [12][13][14][15][16][18][19][20][21][22][23][24][25][26][27][28][29]. The first pleopod-derived prevalence estimates were recorded in 1990 at above 80% [19].…”

“…Patent infection of Nephrops (and other decapods) with Hematodinium sp. appears fatal—possibly due to a combination of disruption to gas transport, tissue dysoxia, energy depletion or dysregulated immune responses caused by the unchecked proliferation of the parasite in the haemolymph [ 12 , 20 , 21 ]. Hematodinium sp.…”

Hemolymph exosomes inhibit Spiroplasma eriocheiris infection by promoting Tetraspanin‐mediated hemocyte phagocytosis in crab

“…In crustaceans, the involvement of exosomes in antiviral and antibacterial resistance has recently been reported 6,7 . Meanwhile, pathogens also evolve the ability to interfere with exosome biogenesis to evade host immunity 8 . However, the mechanism of how exosomes regulate the host's innate immunity deserves further exploration.…”

“…6,7 Meanwhile, pathogens also evolve the ability to interfere with exosome biogenesis to evade host immunity. 8 However, the mechanism of how exosomes regulate the host's innate immunity deserves further exploration.…”