Perkinsus marinus Raghavendra Yadavalli,1 Kousuke Umeda,1,2 and José A. Fernández Robledo1, * 1 Bigelow Laboratory for Ocean Sciences, Boothbay, ME, USA 2 National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Hokkaido, Japan Filter feeding Some parasite rejected in pseudofeces Parasite released in feces Rectum Gills Crassostrea virginica Decaying oyster Disease progressing Perkinsus marinus trophozoite er Extracellular palintomy Host recognition and entry Epithelium (e.g., gill, mantle) Circulating hemocyte Hemocytes transepithelial migration Hemocyte rupture and parasite release TrendsTrendsininParasitologyParasitology Perkinsus marinus is a facultative intracellular marine protozoan parasite responsible for the Dermo disease in Crassostrea virginica oysters. Associated with mass mortalities in the Gulf Coast and Chesapeake Bay (USA), it remains one of the main hurdles for oyster reef restoration and aquaculture. Oysters take up the parasite by filter-feeding; in the pallial cavity it can be phagocytosed by the hemocytes via CvGal1, gaining access to the internal milieu. Inside the parasitophorous vacuole, the parasite resists oxidative stress and acquires nutrients. Propagation strategies include binary fission, budding, palintomy, and schizogony. Although the effect on humans upon consumption of raw infected oysters has not been studied, humanized HLA-DR4 mice fed with P. marinus do not develop noticeable pathology but elicit systemic immunity. Parasite culture in host-free media, and the use of genetic tools, make it a tractable genetic model and a heterologous expression and vaccine-delivery system. Surface moeity Crassostrea virginica Galectin 1 (CvGal1) Secret Pallial cavity Internal milieu Promote Involvement of CvGal1 and CvSI-1 in parasitemia SP nhibitor (CvSI-1) secreted in digestive gland Serine rotease PmSP PmSP and CvSI-1 omplexParasite engulfment (Infected hemocyte) Circulating hemocyte Perkinsus marinus TrendsTrendsininParasitologyParasitology KEY FACTS: P. marinus is phylogenetically close to dinoflagellates and apicomplexans. Two genomes in the nucleus (86 Mb encoding N23 600 proteins) and mitochondrion, using mRNA trans-splicing with a conserved 21–22 nt spliced leader. With a direct life cycle, trophozoites are released into the water with pseudofeces and feces, or from decaying oysters. It remains controversial whether P. marinus produces zoospores as do other Perkinsus spp. Continuous culture in the absence of host cells and transfection methodology enable the study of physiology, cell biology, and host–parasite interactions. It offers a heterologous expression system for human pathogen genes (e.g., Plasmodium falciparum, Toxoplasma gondii, Cryptosporidium parvum, and Ebola virus). DISEASE FACTS: P. marinus infection is one of the World Organization of Animal Health (OIE)-listed diseases. Once described in the Gulf of México, it is now found in both North and South America. High water temperature is the main environmental clue associated with oyster mass mortalities. A protease inhibitor (CvSI-1) isolated from the plasma of eastern oysters inhibits the parasite's proliferation in vitro and appears to be involved in the resistance to Dermo disease. With numerous chemical inhibitors of in vitro propagation, treatment of diseased oysters in the natural environment remains unrealistic. TAXONOMY AND CLASSIFICATION: PHYLUM: Perkinsozoa CLASS: Perkinsea ORDER: Perkinsida FAMILY: Perkinsidae GENUS: Perkinsus SPECIES: P. marinus *Correspondence: jfernandez-robledo@bigelow.org (J.A. Fernández Robledo). Trends in Parasitology, December 2020, Vol. 36, No. 12 © 2020 Elsevier Ltd. All rights reserved. https://doi.org/10.1016/j.pt.2020.05.002 1013 Trends in Parasitology | Parasite of the Month Acknowledgments National Science Foundation (NSF) 1701480 (J.A.F.R.), National Oceanic and Atmospheric Administration (NOAA) NA15NMF4270303 (J.A.F.R.), and JSPS KAKENHI – Grant-in-Aid for JSPS Fellows 19J00148 (K.U.). Resources www.dfo-mpo.gc.ca/science/aah-saa/diseases-maladies/pmdoy-eng.html www.ncbi.nlm.nih.gov/genome/280 www.atcc.org www.protocols.io Literature 1. Mackin, J.G. et al. (1950) Preliminary note on the occurrence of a new protistan parasite, Dermocystidium marinum n. sp., in Crassostrea virginica (Gmelin). Science 111, 328–329 2. Gauthier, J.D. and Vasta, G.R. (1995) In vitro culture of the Eastern parasite Perkinsus marinus: optimization of the methodology. J. Invertebr. Pathol. 66, 156–168 3. Perkins, F.O. (1996) The structure of Perkinsus marinus (Mackin, Owen, and Collier, 1950) Levine, 1978 with comments on taxonomy and phylogeny of Perkinsus spp. J. Shellfish Res. 15, 67–87 4. Tasumi, S. and Vasta, G.R. (2007) A galectin of unique domain organization from hemocytes of the eastern oyster (Crassostrea virginica) is a receptor for the protistan parasite Perkinsus marinus. J. Immunol. 179, 3086–3098 5. Fernández-Robledo, J.A. et al. (2008) Transfection of the protozoan parasite Perkinsus marinus. Mol. Biochem. Parasitol. 157, 44–53 6. Wijayalath, W. et al. (2014) Humanized HLA-DR4 mice fed with the protozoan pathogen of oysters Perkinsus marinus (Dermo) do not develop noticeable pathology but elicit systemic immunity. PLoS One 9, e87435 7. Cold, E.R. et al. (2017) Transient expression of Plasmodium berghei MSP8 and HAP2 in the Marine protozoan parasite Perkinsus marinus. J. Parasitol. 103, 118–122 8. Sakamoto, H. et al. (2017) Investigation into the physiological significance of the phytohormone abscisic acid in Perkinsus marinus, an oyster parasite harboring a non-photosynthetic plastid. J. Eukaryot. Microbiol. 64, 440–446 9. Lau, Y. et al. (2018) Transepithelial migration of mucosal hemocytes in Crassostrea virginica and potential role in Perkinsus marinus pathogenesis. J. Invertebr. Pathol. 153, 122–129 10. Schott, E.J. et al. (2019) Lacking catalase, a protistan parasite draws on its photosynthetic ancestry to complete an antioxidant repertoire with ascorbate peroxidase. BMC Evol. Biol. 19, 146 1014 Trends in Parasitology, December 2020, Vol. 36, No. 12 © 2020 Elsevier Ltd. All rights reserved. https://doi.org/10.1016/j.pt.2020.05.002 Trends in Parasitology | Parasite of the Month