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.

Keywords: Parvilucifera; Perkinsus; X-cell parasite; broad host range parasite; emerging diseases; opportunistic parasite; severe Perkinsea infection.

FIGURE 1

Specificity index within the Perkinsea members. (A) Class of specificity index adapted from Desdevises et al. (2002) and Šimková et al. (2006). Specialists and intermediate specialists are considered as narrow host range (NHR), whereas intermediate generalists, generalists, and “true” generalists are considered as broad host range (BHR). (B) Schematic phylogenies of Parviluciferaceae, Perkinsidae, Xcellidae, and SPI agent where each species was affiliated to a specificity index class (see Supplementary Table 1 for more details).

FIGURE 2

Major phylogenetic relationships within the Perkinsea and other alveolates. (A) Schematic radiation of Alveolata superphylum (not to scale) based on their rDNA phylogeny adapted from Chambouvet et al. (2020). The basal branch (dotted line) is hypothetical. (B) Maximum likelihood tree investigating the Perkinsea diversity based on 18S rRNA. The phylogeny was calculated from 134 taxa and 1,431 character alignment position. Seven sequences of dinoflagellates, Syndiniales, and MALV (marine alveolate) were used as an outgroup. ML bootstrap values (1,000 replicates, GTR+F+R5) and Bayesian posterior probability (8,000,000 generations, GTR+G+R5 model) were notated using the following convention: support values are summarized by black circles when ≥ 80%/0.9 and white circles when it is not the case but values ≥ 60%/0.6. When the topology is inconsistent in one of the inference methods, it is denoted by a ‘−’ (see phylogenetic analysis details in Supplementary SMM). The sequence origins are represented by squares of colors: light blue for marine waters, yellow for land waters, green for brackish waters, and red for wetland soil. Purple asterisks indicate host-associated sequences. The tree was annotated using Interactive Tree of Life (IToL) (https://itol.embl.de/, Letunic and Bork, 2019) and Inkscape (https://inkscape.org/en/).

FIGURE 3

Geographical distribution of Perkinsea parasitic protist based on scientific literature from 1950 to 2020. Detection provenance of (A) Perkinsidae, (B) Parviluciferaceae, (C) Xcellidae family, and (D) SPI agent (detail of selected references in Supplementary Table 1) is indicated by a colored triangle when the parasite is detected simultaneously by molecular (qPCR or PCR) and microscopic methodologies (histology or RFTM incubation or cultures), and by a star when presence of the parasitic protists was linked to a mortality event. The color of triangles or stars designates the parasite species (see key). World map drawing is a free public domain vector cliparts (available at https://commons.wikimedia.org).

FIGURE 4

Cartoon illustration of the described life cycle of Perkinsea. Drawing representing the life cycle of (A) Perkinsus olseni infecting its clam host [adapted from Auzoux-Bordenave et al. (1996)] and of (B) Parvilucifera sinerae infecting its dinoflagellate host [adapted from Alacid et al. (2015)].