Emerging Parasitic Protists: The Case of Perkinsea

Abstract

The last century has witnessed an increasing rate of new disease emergence across the world leading to permanent loss of biodiversity. Perkinsea is a microeukaryotic parasitic phylum composed of four main lineages of parasitic protists with broad host ranges. Some of them represent major ecological and economical threats because of their geographically invasive ability and pathogenicity (leading to mortality events). In marine environments, three lineages are currently described, the Parviluciferaceae, the Perkinsidae, and the Xcellidae, infecting, respectively, dinoflagellates, mollusks, and fish. In contrast, only one lineage is officially described in freshwater environments: the severe Perkinsea infectious agent infecting frog tadpoles. The advent of high-throughput sequencing methods, mainly based on 18S rRNA assays, showed that Perkinsea is far more diverse than the previously four described lineages especially in freshwater environments. Indeed, some lineages could be parasites of green microalgae, but a formal nature of the interaction needs to be explored. Hence, to date, most of the newly described aquatic clusters are only defined by their environmental sequences and are still not (yet) associated with any host. The unveiling of this microbial black box presents a multitude of research challenges to understand their ecological roles and ultimately to prevent their most negative impacts. This review summarizes the biological and ecological traits of Perkinsea—their diversity, life cycle, host preferences, pathogenicity, and highlights their diversity and ubiquity in association with a wide range of hosts.

A diversified and segregated mRNA spliced-leader system in the parasitic Perkinsozoa

“…The high similarity between Perkinsus and dinoflagellates regarding SLe length and nucleotide composition, suggests that the evolution of longer SLe forms encompassing adenine-enriched insertions seen in M. nigrum and P. sinerae occurred during the evolution of Perkinsozoa, leading to the increased diversification of SL-types (figures 1 and 2). This pattern of SL-sequence variation is consistent with the branch-lengths observed for the concatenated small subunit (SSU) and large subunit (LSU) rRNA gene phylogenies (figure 2c), in agreement with previous phylogenetic analysis [16,18,19,21] where the Perkinsozoa, specifically M. nigrum and P. sinerae, demonstrate divergent patterns of rRNA sequence variation. We note here that the SSU/LSU rRNA gene phylogeny is shown primarily to contrast the patterns of rRNA sequence variation with variation in the S4).…”

Microscopic marine invertebrates are reservoirs for cryptic and diverse protists and fungi

“…Perkinsea are alveolate parasites that can cause mass mortality events in fish, molluscs, and amphibians [91]. We detected a single perkinsid ASV in seven microscopic invertebrate specimens (two annelids, two molluscs, and three arthropods) (Fig.…”

A parasite outbreak in notothenioid fish in an Antarctic fjord

“…The large cells were histologically similar to those previously identified in X-cell disease ( Bucke and Everson, 1992 ; Freeman et al., 2017 ), whereas the smaller cells resembled host fibroblasts, together forming multiple xenoparasitic complexes ( Figure 2 F). X-cell disease affects various fish groups throughout the world ( Bucke and Everson, 1992 ; Davison, 1997 ; Diamant et al., 1994 ; Evans and Tupmongkol, 2014 ; Freeman et al., 2011 , 2017 ; Freeman, 2009 ; Karlsbakk et al., 2021 ; Miwa and Kamaishi, 2009 ) and is caused by a parasitic alveolate of the family Xcellidae that is related to the bivalve parasite Perkinsus ( Freeman et al., 2017 ; Itoïz et al, 2022 ).…”

“…Many knowledge gaps persist about X-cell disease, including the life cycle of X-cell parasites ( Freeman et al., 2011 ), confirmation of their possible transmission by contact of the fish with the benthic substrate ( Freeman et al., 2017 ), potential biotic and abiotic reservoirs, host ranges (i.e., the number of host species for a given parasite species), host-parasite interactions, and biogeographic distribution of the various X-cell lineages ( Itoïz et al, 2022 ). It cannot be excluded, however, that the outbreak may expand within this population, spread to other localities, and potentially infect other species.…”