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Research Article

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

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Article: 2180932 | Received 21 Nov 2022, Accepted 12 Feb 2023, Published online: 02 Mar 2023

References

  • Ens NJ, Harvey B, Davies MM, et al. The Green Wave: reviewing the environmental impacts of the invasive European green crab (Carcinus maenas) and potential management approaches. Environ Rev. 2022;30(2):306–12.
  • Walton WC, MacKinnon C, Rodriguez LF, et al. Effect of an invasive crab upon a marine fishery: green crab, Carcinus maenas, predation upon a venerid clam, Katelysia scalarina, in Tasmania (Australia). J Exp Mar Biol Ecol. 2002;272(2):171–189.
  • Bojko J, Stebbing PD, Dunn AM, et al. Green crab Carcinus maenas symbiont profiles along a North Atlantic invasion route. Dis Aquat Organ. 2018;128(2):147–168.
  • Rowley AF, Davies CE, Malkin SH, et al. Prevalence and histopathology of the parasitic barnacle, Sacculina carcini in shore crabs, Carcinus maenas. J Invertebr Pathol. 2020;171:107338.
  • Zetlmeisl C, Hermann J, Petney T, et al. Parasites of the shore crab Carcinus maenas (L.): implications for reproductive potential and invasion success. Parasitology. 2011;138(3):394–401.
  • Davies CE, Batista FM, Malkin SH, et al. Spatial and temporal disease dynamics of the parasite Hematodinium sp. in shore crabs, Carcinus maenas. Parasit Vectors. 2019;12(1):1–15.
  • Davies CE, Thomas JE, Malkin SH, et al. Hematodinium sp. infection does not drive collateral disease contraction in a crustacean host. Elife. 2022;11:e70356.
  • Bookelaar BE, Reilly AO, Lynch SA, et al. Role of the intertidal predatory shore crab Carcinus maenas in transmission dynamics of ostreid herpesvirus-1 microvariant. Dis Aquat Organ. 2018;130(3):221–233.
  • Davies CE, Bass D, Ward GM, et al. Diagnosis and prevalence of two new species of haplosporidians infecting shore crabs Carcinus maenas: Haplosporidium carcini n. sp., and H. cranc n. sp. Parasitology. 2020a;147(11):1229–1237.
  • Gong M, Xie G, Wang H, et al. Hematodinium perezi naturally infects Asian brush‐clawed crab (Hemigrapsus takanoi). J Fish Dis. 2022;46(1):67–74. in press. DOI:10.1111/jfd.13718.
  • Gornik SG, Cranenburgh A, Waller RF. New host range for Hematodinium in southern Australia and novel tools for sensitive detection of parasitic dinoflagellates. PLoS ONE. 2013;8(12):e82774.
  • Stentiford GD, Shields JD. A review of the parasitic dinoflagellates Hematodinium species and Hematodinium-like infections in marine crustaceans. Dis Aquat Organ. 2005;66(1):47–70.
  • Messick GA, Hematodinium perezi infections in adult and juvenile blue crabs Callinectes sapidus from coastal bays of Maryland and Virginia, USA. Dis Aquat Organ. 1994;19: 77-77. DOI:10.3354/dao019077.
  • Small HJ, Huchin-Mian JP, Reece KS, et al. Parasitic dinoflagellate Hematodinium perezi prevalence in larval and juvenile blue crabs Callinectes sapidus from coastal bays of Virginia. Dis Aquat Organ. 2019;134(3):215–222.
  • Albalat A, Collard A, Brucem C, et al. Physiological condition, short-term survival, and predator avoidance behavior of discarded Norway lobsters (Nephrops norvegicus). J Shellfish Res. 2016;35(4):1053–1065.
  • Albalat A, Gornik SG, Beevers N, et al. Hematodinium sp. infection in Norway lobster Nephrops norvegicus and its effects on meat quality. Dis Aquat Organ. 2012;100(2):105–112.
  • Stentiford GD, Neil DM, Atkinson RJA. The relationship of Hematodinium infection prevalence in a Scottish Nephrops norvegicus population to season, moulting and sex. ICES J Mar Sci. 2001;58(4):814–823.
  • Smith AL, Hamilton KM, Hirschle L, et al. Characterization and molecular epidemiology of a fungal infection of edible crabs (Cancer pagurus) and interaction of the fungus with the dinoflagellate parasite Hematodinium. Appl environ microbiol. 2013;79(3):783–793.
  • Smith AL, Hirschle L, Vogan CL, et al. Parasitization of juvenile edible crabs (Cancer pagurus) by the dinoflagellate, Hematodinium sp.: pathobiology, seasonality and its potential effects on commercial fisheries. Parasitology. 2015;142(3):428–438.
  • Crandall G, Jensen PC, White SJ, et al. Characterization of the gene repertoire and environmentally driven expression patterns in Tanner crab (Chionoecetes bairdi). Mar Biotechnol. 2022;24(1):216–225.
  • Jensen PC, Califf K, Lowe V, et al. Molecular detection of Hematodinium sp. in Northeast Pacific Chionoecetes spp. and evidence of two species in the Northern Hemisphere. Dis Aquat Organ. 2010;89(2):155–166.
  • Xu W, Xie J, Shi H, et al. Hematodinium infections in cultured ridgetail white prawns, Exopalaemon carinicauda, in eastern China. Aquaculture. 2010;300(1–4):25–31.
  • Li M, Huang Q, Lv X, et al. The parasitic dinoflagellate Hematodinium infects multiple crustaceans in the polyculture systems of Shandong Province, China. J Invertebr Pathol. 2021;178:107523.
  • Coates CJ, Rowley A. Emerging diseases and epizootics in crabs under cultivation. Front Mar Sci. 2022;8:e809759.
  • Chisholm JR, Smith VJ. Antibacterial activity in the haemocytes of the shore crab, Carcinus maenas. J Mar Biol Assoc UK. 1992;72(3):529–542.
  • Coates CJ, Nairn J. Diverse immune functions of hemocyanins. Dev Comp Immunol. 2014;45(1):43–55.
  • Hauton C, Williams JA, Hawkins LE. The effects of a live in vivo pathogenic infection on aspects of the immunocompetence of the common shore crab, Carcinus maenas (L.). J Exp Mar Biol Ecol. 1997;211(1):115–128.
  • Powell A, Rowley AF. The effect of dietary chitin supplementation on the survival and immune reactivity of the shore crab, Carcinus maenas. Comp Biochem Physiol Part A: Mol Integr Physiol. 2007;147(1):122–128.
  • Suleiman S, Smith VJ, Dyrynda EA. Unusual tissue distribution of carcinin, an antibacterial crustin, in the crab, Carcinus maenas, reveals its multi-functionality. Dev Comp Immunol. 2017;76:274–284.
  • Rowley AF, Smith AL, Davies CE. How does the dinoflagellate parasite Hematodinium outsmart the immune system of its crustacean hosts? PLOS Pathogens. 2015;11(5):e1004724.
  • Li M, Huang Q, Lv X, et al. Integrative omics analysis highlights the immunomodulatory effects of the parasitic dinoflagellate Hematodinium on crustacean hemocytes. Fish Shellfish Immunol. 2022;125:35–47.
  • Li M, Wang J, Huang Q, et al. Proteomic analysis highlights the immune responses of the hepatopancreas against Hematodinium infection in Portunus trituberculatus. J Proteomics. 2019;197:92–105.
  • Bielecka E, Scavenius C, Kantyka T, et al. Peptidyl arginine deiminase from Porphyromonas gingivalis abolishes anaphylatoxin C5a activity. J Biol Chem. 2014;289(47):32481–32487.
  • El-Sayed AS, Shindia AA, AbouZaid AA, et al. Biochemical characterization of peptidylarginine deiminase-like orthologs from thermotolerant Emericella dentata and Aspergillus nidulans. Enzyme Microb Technol. 2019;124:41–53.
  • Gavinho B, Sabatke B, Feijoli V, et al. Peptidylarginine deiminase inhibition abolishes the production of large extracellular vesicles from Giardia intestinalis, affecting host-pathogen interactions by hindering adhesion to host cells. Front Cell Infect Microbiol. 2020;10:417.
  • Kosgodage US, Matewele P, Mastroianni G, et al. Peptidylarginine deiminase inhibitors reduce bacterial membrane vesicle release and sensitize bacteria to antibiotic treatment. Front Cell Infect Microbiol. 2019;9:227.
  • Novák L, Zubáčová Z, Karnkowska A, et al. Arginine deiminase pathway enzymes: evolutionary history in metamonads and other eukaryotes. BMC Evol Biol. 2016;16(1):1–14.
  • Kristmundsson Á, Erlingsdóttir Á, Lange S. Peptidylarginine deiminase (PAD) and post-translational protein deimination—novel insights into Alveolata metabolism, epigenetic regulation and host–pathogen interactions. Biology (Basel). 2021;10(3):177.
  • Bowden TJ, Kraev I, Lange S. Post-translational protein deimination signatures and extracellular vesicles (EVs) in the Atlantic horseshoe crab (Limulus polyphemus). Dev Comp Immunol. 2020a;110:103714.
  • Bowden TJ, Kraev I, Lange S. Extracellular vesicles and post-translational protein deimination signatures in haemolymph of the American lobster (Homarus americanus). Fish Shellfish Immunol. 2020b;106:79–102.
  • Bowden TJ, Kraev I, Lange S. Extracellular vesicles and post-translational protein deimination signatures in mollusca—the blue mussel (Mytilus edulis), soft shell clam (Mya arenaria), Eastern Oyster (Crassostrea virginica) and Atlantic Jacknife Clam (Ensis leei). Biology (Basel). 2020c;9(12):416.
  • D’alessio S, Buckley KM, Kraev I, et al. Extracellular vesicle signatures and post-translational protein deimination in purple sea urchin (Strongylocentrotus purpuratus) coelomic fluid—novel insights into echinodermata biology. Biology (Basel). 2021;10(9):866.
  • Magnadóttir B, Uysal-Onganer P, Kraev I, et al. Extracellular vesicles, deiminated protein cargo and microRnas are novel serum biomarkers for environmental rearing temperature in Atlantic cod (Gadus morhua L.). Aquac Rep. 2020;16:100245.
  • Gruebl T, Frischer ME, Sheppard M, et al. Development of an 18S rRNA gene targeted PCR based diagnostic for the blue crab parasite Hematodinium sp. Dis Aquat Organ. 2002;49(1):61–70.
  • Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750. DOI:10.1080/20013078.2018.1535750
  • Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9(7):671–675.
  • Cummings TF, Gori K, Sanchez-Pulido L, et al. Citrullination was introduced into animals by horizontal gene transfer from cyanobacteria. Mol Biol Evol. 2022;39(2):msab317.
  • Li M, Wang J, Song S, et al. Early transcriptional response to the parasitic dinoflagellate Hematodinium in hepatopancreas of Portunus trituberculatus. J Invertebr Pathol. 2015;130:28–36.
  • Stentiford GD, Evans M, Bateman K, et al. Co-infection by a yeast-like organism in Hematodinium-infected European edible crabs Cancer pagurus and velvet swimming crabs Necora puber from the English Channel. Dis Aquat Organ. 2003;54(3):195–202.
  • Carton Y, Poirié M, Nappi AJ. Insect immune resistance to parasitoids. Insect Sci. 2008;15(1):67–87.
  • Li M, Wang J, Song S, et al. Molecular characterization of a novel nitric oxide synthase gene from Portunus trituberculatus and the roles of NO/O2−-generating and antioxidant systems in host immune responses to Hematodinium. Fish Shellfish Immunol. 2016;52:263–277.
  • Li XJ, Yang L, Li D, et al. Pathogen-specific binding soluble down syndrome cell adhesion molecule (Dscam) regulates phagocytosis via membrane-bound Dscam in crab. Front Immunol. 2018;9:801.
  • Ng TH, Kurtz J. Dscam in immunity: a question of diversity in insects and crustaceans. Dev Comp Immunol. 2020;105:103539.
  • Robb CT, Dyrynda EA, Gray RD, et al. Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon. Nat Commun. 2014;5(1):1–11.
  • Brockton V, Hammond JA, Smith VJ. Gene characterisation, isoforms and recombinant expression of carcinin, an antibacterial protein from the shore crab, Carcinus maenas. Mol Immunol. 2007;44(5):943–949.
  • Davies CE, Malkin SH, Thomas JE, et al. Mycosis is a disease state encountered rarely in shore crabs, Carcinus maenas. Pathogens. 2020b;9(6):462.
  • Coates CJ, Costa-Paiva EM. Multifunctional roles of hemocyanins. In: Hoeger U, and JR Harris, editors. Vertebrate and invertebrate respiratory proteins, lipoproteins and other body fluid proteins. Switzerland: Springer Nature; 2020. p. 233–250.