Myxozoan polar tubules display structural and functional variation

Abstract

BackgroundMyxozoa is a speciose group of endoparasitic cnidarians that can cause severe ecological and economic effects. Although highly reduced compared to free-living cnidarians, myxozoans have retained the phylum-defining stinging organelles, known as cnidae or polar capsules, which are essential to initiating host infection. To explore the adaptations of myxozoan polar capsules, we compared the structure, firing process and content release mechanism of polar tubules in myxospores of three Myxobolus species including M. cerebralis, the causative agent of whirling disease.ResultsWe found novel functions and morphologies in myxozoan polar tubules. High-speed video analysis of the firing process of capsules from the three Myxobolus species showed that all polar tubules rapidly extended and then contracted, an elasticity phenomenon that is unknown in free-living cnidarians. Interestingly, the duration of the tubule release differed among the three species by more than two orders of magnitude, ranging from 0.35 to 10 s. By dye-labeling the polar capsules prior to firing, we discovered that two of the species could release their entire capsule content, a delivery process not previously known from myxozoans. Having the role of content delivery and not simply anchoring suggests that cytotoxic or proteolytic compounds may be present in the capsule. Moreover, while free-living cnidarians inject most of the toxic content through the distal tip of the tubule, our video and ultrastructure analyses of the myxozoan tubules revealed patterns of double spirals of nodules and pores along parts of the tubules, and showed that the distal tip of the tubules was sealed. This helical pattern and distribution of openings may minimize the tubule mechanical weakness and improve resistance to the stress impose by firing. The finding that myxozoan tubule characteristics are very different from those of free-living cnidarians is suggestive of their adaptation to parasitic life.ConclusionsThese findings show that myxozoan polar tubules have more functions than previously assumed, and provide insight into their evolution from free-living ancestors.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1819-4) contains supplementary material, which is available to authorized users.

Functional and proteomic analysis of Ceratonova shasta (Cnidaria: Myxozoa) polar capsules reveals adaptations to parasitism

“…Myxozoans typically have only two or three polar capsules, which are essential for the initiation of host infection. The fired tubule anchors the spore to the host, in some cases by contracting to achieve closer contact, and subsequently injecting the capsule content 24 – 26 . The first myxozoan whole-genome data contain genes encoding capsule-specific structural proteins, including minicollagens and nematogalectins 13 ; however, little is known of the composition of the polar capsule content, and if it shares any similarity to nematocysts of free-living cnidarians, despite the organelles having different functions.…”

Insights into myxozoan composition and physiology revealed by histochemical properties of myxospores

“…Another possible role of intracapsular calcium may involve host invasion. Injection of calcium, or other cytotoxic contents, into host epithelial cells could potentially cause dysregulation of intracellular calcium and initiate cellular apoptosis (Ben‐David et al, 2016). The resulting defect in the epithelial barrier could facilitate penetration of the annelid intestinal mucosa by the infective sporoplasm.…”

“…Their morphology reflects a markedly simplified form of their evolutionary origins within the phylum Cnidaria (Atkinson et al, 2018). In particular, the myxozoan polar capsule is compared to the cnidarian nematocyst in form and function (Ben‐David et al, 2016; Cannon & Wagner, 2003). The polar filament, ejected from the capsule upon contact with host mucin, attaches to the host and retracts to bring the spore and host into close proximity (Ben‐David et al, 2016; Kallert, Ponader, Eszterbauer, El‐Matbouli, & Haas, 2007).…”

“…In particular, the myxozoan polar capsule is compared to the cnidarian nematocyst in form and function (Ben‐David et al, 2016; Cannon & Wagner, 2003). The polar filament, ejected from the capsule upon contact with host mucin, attaches to the host and retracts to bring the spore and host into close proximity (Ben‐David et al, 2016; Kallert, Ponader, Eszterbauer, El‐Matbouli, & Haas, 2007). Additionally, myxospores may inject cytotoxic contents of the polar capsule into the host (Ben‐David et al, 2016).…”

“…The polar filament, ejected from the capsule upon contact with host mucin, attaches to the host and retracts to bring the spore and host into close proximity (Ben‐David et al, 2016; Kallert, Ponader, Eszterbauer, El‐Matbouli, & Haas, 2007). Additionally, myxospores may inject cytotoxic contents of the polar capsule into the host (Ben‐David et al, 2016). Most myxozoans are not highly pathogenic, but some cause significant tissue destruction, morbidity and mortality in their fish hosts (Hedrick et al, 2003; Sterud et al, 2007).…”