Integrative omics analysis highlights the immunomodulatory effects of the parasitic dinoflagellate Hematodinium on crustacean hemocytes

Li, Meng; Huang, Qian; Lv, Xiaoyang; Small, Hamish J.; Li, Caiwen

doi:10.1016/j.fsi.2022.04.050

Cited by 5 publications

(3 citation statements)

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“…isolated from donor (diseased) crabs did not display typical signs of cell-derived immunity (no degranulation, phagocytosis, or encapsulation [ 7 ]). Conversely, in gazami crabs ( P. trituberculatus ) infected with H. perezi under laboratory conditions, there is evidence that the host does respond to the dinoflagellate at the mRNA and protein levels – changes in candidate immune gene/protein expression, such as, pro-phenoloxidase or miRNAs [ 31 , 32 , 48 ] – yet findings are inconsistent. In Li et al [ 48 ], enzyme activities (phenoloxidase, acid and alkaline phosphatases) in the hepatopancreas of H. perezi infected P. trituberculatus were elevated over 6–192 hours post infection when compared to control crabs, whereas in Li et al [ 31 ] the pro-phenoloxidase activation pathway was significantly downregulated (revealed by multi-omics techniques) as was haemocyte phenoloxidase enzyme activity over the same time frame.…”

Section: Discussionmentioning

confidence: 99%

“…The modulation of actin can also disrupt phagosome formation. Out of all the immune-related pathways investigated in Hematodinium- infected P. trituberculatus by Li et al [ 31 ], “regulation of the actin cytoskeleton” and “focal adhesion” were the two most enriched (up to 14-fold). As such, Hematodinium -driven post-translational modification could be a mechanism of immune interference.…”

Section: Discussionmentioning

confidence: 99%

“…influence crab immunity [ 30 ]. For gazami crabs ( P. trituberculatus ) infected with H. perezi , Li et al [ 31 , 32 ] applied multi-omic approaches to the hepatopancreas and haemolymph (containing haemocytes), revealing potential immune-suppressive strategies of the dinoflagellate in a bid to colonize the host, such as, disrupting phagosome formation. To the best of our knowledge, no Hematodinium -derived factor has been identified to date with a direct immune-suppressive role.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2023

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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.

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