Evidence from the resurrected family Polyrhabdinidae Kamm, 1922 (Apicomplexa: Gregarinomorpha) supports the epimerite, an attachment organelle, as a major eugregarine innovation

Abstract

Background Gregarines are a major group of apicomplexan parasites of invertebrates. The gregarine classification is largely incomplete because it relies primarily on light microscopy, while electron microscopy and molecular data in the group are fragmentary and often do not overlap. A key characteristic in gregarine taxonomy is the structure and function of their attachment organelles (AOs). AOs have been commonly classified as “mucrons” or “epimerites” based on their association with other cellular traits such as septation. An alternative proposal focused on the AOs structure, functional role, and developmental fate has recently restricted the terms “mucron” to archigregarines and “epimerite” to eugregarines. Methods Light microscopy and scanning and transmission electron microscopy, molecular phylogenetic analyses of ribosomal RNA genes. Results We obtained the first data on fine morphology of aseptate eugregarines Polyrhabdina pygospionis and Polyrhabdina cf. spionis, the type species. We demonstrate that their AOs differ from the mucron in archigregarines and represent an epimerite structurally resembling that in other eugregarines examined using electron microscopy. We then used the concatenated ribosomal operon DNA sequences (SSU, 5.8S, and LSU rDNA) of P. pygospionis to explore the phylogeny of eugregarines with a resolution superior to SSU rDNA alone. The obtained phylogenies show that the Polyrhabdina clade represents an independent, deep-branching family in the Ancoroidea clade within eugregarines. Combined, these results lend strong support to the hypothesis that the epimerite is a synapomorphic innovation of eugregarines. Based on these findings, we resurrect the family Polyrhabdinidae Kamm, 1922 and erect and diagnose the family Trollidiidae fam. n. within the superfamily Ancoroidea Simdyanov et al., 2017. Additionally, we re-describe the characteristics of P. pygospionis, emend the diagnoses of the genus Polyrhabdina, the family Polyrhabdinidae, and the superfamily Ancoroidea.

Diversity, Distribution and Development of Hyperparasitic Microsporidia in Gregarines within One Super-host

“…Our studies [55][56], and the observations performed by Hiillos with co-authors [57] showed that the gregarines were widely distributed in the populations of P. elegans, where most polychaete specimens harbored these parasites. Authors also noted that the variation in the prevalence of gregarines between polychaete populations, characteristic of S. pygospionis and P. pygospionis, is a common feature of parasitic apicomplexans.…”

“…According to an alternative idea, the sporoplasm causes invagination of the host plasma membrane in the contact zone between the manubrium and the area of a gregarine micropore, where the pellicle is thin [30], [34]. It should be noted that archigregarines S. pygospionis and eugregarines P. pygospionis have numerous micropores on their cell surface, at the bottom of cortical grooves and on the sides of epicytic folds, respectively [55][56]. A similar mechanism of invagination of the host plasma membrane in the contact zone between the penetration tube and the host cell (a kind of invasion synapse) is suggested for aphelids, holomycotan parasitoids of algae, closely related to fungi, and Rozella spp., parasitoids of zoosporic fungi and oomycetes, closely related to microsporidia [59].…”

Droplet digital PCR as a tool for investigating dynamics of cryptic symbionts

“…This species can be a dominant member of benthic communities (Bolam, 2004; Bolam & Fernandes, 2003) and is an important prey item for other invertebrates and fish (Mattila, 1997). Pygospio elegans is known to host at least two apicomplexan symbionts: the archigregarine Selenidium pygospionis (Paskerova et al, 2018) and the eugregarine Polyrhabdina pygospionis (Paskerova et al, 2021), which both inhabit the worm's intestine. In our previous study of the host's transcriptome (Heikkinen et al, 2017), we detected the presence of a third apicomplexan symbiont.…”

“…Amplification efficiency of the primers was estimated to be 94.3% (slope = −3.465, r 2 = .997) using a qPCR. To demonstrate the specificity of the designed primers, the assay was checked against other apicomplexan DNA that might be present in the host gut; S. pygospionis (Archigregarinorida) (Paskerova et al, 2018) and P. pygospionis (Eugregarinorida) (Paskerova et al, 2021). Individual S. pygospionis ( n = 88) and P. pygospionis ( n = 33) cells were isolated from P. elegans collected in September 2020 (St. Petersburg, Russia).…”

Diversity, Distribution, and Development of Hyperparasitic Microsporidia in Gregarines within One Super-Host

“…Many studies also demonstrated no effect at all [ 54 ]. Our studies [ 55 , 56 ], and the observations performed by Hiillos with co-authors [ 57 ], showed that the gregarines were widely distributed in P. elegans populations, in which most polychaete specimens harbored these parasites. The prevalence of gregarines S. pygospionis and P. pygospionis varied among populations of polychaetes, which is a common feature of apicomplexan parasites [ 57 ].…”