How does the dinoflagellate parasite Hematodinium outsmart the immune system of its crustacean hosts?

Abstract

Dinoflagellates of the genusHematodinium infect over 40 species of marine crustaceans. Since the initial description of this parasite in France in the 1930s [1], it appears to have spread globally, causing economic loss in some species, including Tanner crabs (Chionoecetes bairdi) in Alaska [2], blue crabs (Callinectes sapidus) in the United States [3], edible crabs (Cancer pagurus) and Norway lobsters (Nephrops norvegicus) in Europe [4–7], sand crabs (Portunus armatus) in Australia [8], and Chinese swimming crabs (Portunus trituberculatus) in northern China [9]. Because this disease is thought to be fatal, it may be of great significance to the sustainability of both captive shellfish fisheries and aquaculture [10,11]. For instance, the decline in blue crabs from the Atlantic to Gulf Coasts in the US appears to be linked to epizootic outbreaks of disease caused byHematodinium [12]. Similarly, the reduction in velvet swimmer crab (Necora puber) numbers in Brittany in the 1980s has been attributed to the high prevalence of such infections [13]. Finally, the recent reports ofHematodinium infections in crabs and shrimp raised under aquaculture conditions in China [9,14,15] highlight the danger to additional, cultured crustacean populations. The number and host range of species ofHematodinium is unclear. Chatton and Poisson [1] identified one species of this parasite that they termed H. perezi. Notably, this species of parasite was reported in two different species of crabs from several locations around the French coast. A second species,H. australis, was first described in sand crabs fromMoreton Bay in Australia [8]. Recent studies making use of the variability of the ITS1 rDNA region ofH. perezi suggest that there are three clades (genotypes), I–III, of this species (see [11] for further details). Pagenkopp Lohan et al. [16] concluded that blue crab populations collected from the Atlantic to the Gulf coasts of the US were all affected by one genotype, H. perezi (III), which implies a large geographic range. Importantly, other species of crabs collected from the same region were also infected by the same genotype of H. perezi [16]. In Europe, there may be two clades of Hematodinium infecting a range of crabs. H. perezi genotype I has been reported in Liocarcinus depurator [17] and Carcinus maenas. The second species ofHematodinium, currently unnamed (Hematodinium sp.) infects a wider range of crustaceans, including edible crabs (C. pagurus). Importantly, these observations imply that this parasite is a host generalist and may be able to “jump” from host species to species, thereby making it a significant threat to a wide variety of commercially important decapods.