Hyperspora aquatica n.gn., n.sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa

Abstract

The Paramyxida, closely related to haplosporidians, paradinids, and mikrocytids, is an obscure order of parasitic protists within the class Ascetosporea. All characterized ascetosporeans are parasites of invertebrate hosts, including molluscs, crustaceans and polychaetes. Representatives of the genus Marteilia are the best studied paramyxids, largely due to their impact on cultured oyster stocks, and their listing in international legislative frameworks. Although several examples of microsporidian hyperparasitism of paramyxids have been reported, phylogenetic data for these taxa are lacking. Recently, a microsporidian parasite was described infecting the paramyxid Marteilia cochillia, a serious pathogen of European cockles. In the current study, we investigated the phylogeny of the microsporidian hyperparasite infecting M. cochillia in cockles and, a further hyperparasite, Unikaryon legeri infecting the digenean Meiogymnophallus minutus, also in cockles. We show that rather than representing basally branching taxa in the increasingly replete Cryptomycota/Rozellomycota outgroup (containing taxa such as Mitosporidium and Paramicrosoridium), these hyperparasites instead group with other known microsporidian parasites infecting aquatic crustaceans. In doing so, we erect a new genus and species (Hyperspora aquatica n. gn., n.sp.) to contain the hyperparasite of M. cochillia and clarify the phylogenetic position of U. legeri. We propose that in both cases, hyperparasitism may provide a strategy for the vectoring of microsporidians between hosts of different trophic status (e.g. molluscs to crustaceans) within aquatic systems. In particular, we propose that the paramyxid hyperparasite H. aquatica may eventually be detected as a parasite of marine crustaceans. The potential route of transmission of the microsporidian between the paramyxid (in its host cockle) to crustaceans, and, the 'hitch-hiking' strategy employed by H. aquatica is discussed.

Clarifying the Relationships between Microsporidia and Cryptomycota

“…The nr nucleotide GenBank database was blastn searched using seed SSU rRNA gene sequences of characterized microsporidia‐like protists, metchnikovellids, deeply branching LB‐Microsporidia (clades 2 and 3 Stentiford et al. ), and the phylogenetic diversity of “Cryptomycota” and aphelids in Karpov et al. ().…”

“…The nr nucleotide GenBank database was blastn searched using seed SSU rRNA gene sequences of characterized microsporidia-like protists, metchnikovellids, deeply branching LB-Microsporidia (clades 2 and 3 Stentiford et al 2017), and the phylogenetic diversity of "Cryptomycota" and aphelids in Karpov et al (2014). The top 50 matches for each sequence were downloaded, aligned with mafft e-ins-i (Katoh and Standley 2013), deduplicated, and a preliminary tree constructed on the basis of which the number of closely related sequences was reduced, retaining the longest possible sequences.…”

“…Published phylogenies (e.g. Stentiford et al 2017) show that these form a very robust monophyletic group with all other LB-Microsporidia, so it is reasonable to use them as a proxy for the whole group in this study. A Bayesian phylogeny was inferred under the CAT+GTR+Gamma (4) model in PhyloBayes-MPI 1.7 (Lartillot et al 2013).…”

“…), and hyperparasites in protists: metchnikovellids are parasites of gregarines, protistan gut symbionts of many invertebrates, and Hyperspora aquatica is a hyperparasite of the paramyxid Marteilia cochillia , a serious pathogen of European cockles (Stentiford et al. ). Rozella species are zoosporic biotrophic parasites of oomycetes, chytrids, and Blastocladiomycota (Spatafora et al.…”

“…Microsporidia are known primarily as parasites of invertebrates and vertebrates (including humans), but are also known as endosymbionts of ciliates (Fokin 2012;Fokin et al 2008), and hyperparasites in protists: metchnikovellids are parasites of gregarines, protistan gut symbionts of many invertebrates, and Hyperspora aquatica is a hyperparasite of the paramyxid Marteilia cochillia, a serious pathogen of European cockles (Stentiford et al 2017). Rozella species are zoosporic biotrophic parasites of oomycetes, chytrids, and Blastocladiomycota (Spatafora et al 2017).…”