Myxozoa is a diverse, speciose group of microscopic parasites, recently placed within the phylum Cnidaria. Myxozoans are highly reduced in size and complexity relative to free-living cnidarians, yet they have retained specialized organelles known as polar capsules, akin to the nematocyst stinging capsules of free-living species. Whereas in free-living cnidarians the stinging capsules are used for prey capture or defense, in myxozoans they have the essential function of initiating the host infection process. To explore the evolutionary adaptation of polar capsules to parasitism, we used as a model organism Ceratonova shasta, which causes lethal disease in salmonids. Here, we report the first isolation of C. shasta myxospore polar capsules using a tailored dielectrophoresis-based microfluidic chip. Using electron microscopy and functional analysis we demonstrated that C. shasta tubules have no openings and are likely used to anchor the spore to the host. Proteomic analysis of C. shasta polar capsules suggested that they have retained typical structural and housekeeping proteins found in nematocysts of jellyfish, sea anemones and Hydra, but have lost the most important functional group in nematocysts, namely toxins. Our findings support the hypothesis that polar capsules and nematocysts are homologous organelles, which have adapted to their distinct functions.

These authors contributed equally to this study.Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.3693214.

Jellyfish stinging capsules known as nematocysts are explosive, natural-injection systems with high potential as a natural drug-delivery system. These organelles consist of a capsule containing a highly folded thin needle-like tubule and a matrix highly concentrated with charged constituents that enable the tubule to fire and penetrate a target. For the purpose of using these nematocysts as drug delivery system it is first required to purify subpopulations from heterogeneous population of capsules and to investigate each subpopulation's distinct function and characteristics. Here, the nematocysts' dielectric properties were experimentally investigated using dielectrophoretic and electrorotational spectra with best fits derived from theoretical models. The dielectric characterization adds to our understanding of the nematocysts' structure and function and is necessary for the dielectrophoretic isolation and manipulation of populations. As expected, the effect of monovalent and divalent exchange cations resulted in higher inner conductivity for the NaCl treated capsules; this result stands in agreement with their relative higher osmotic pressure. In addition, an efficient dielectrophoretic isolation of different nematocyst subpopulations was demonstrated, paving the way to an understanding of nematocysts' functional diversity and the development of an efficient drug delivery platform.

Electrophoresis 2017, 38, 1996–2003. DOI: https://doi.org/10.1002/elps.201700072 The front cover picture shows the dielectric characterization of jellyfish stinging capsules using a quadrupole microelectrode array in terms of dielectrophoretic (DEP) and electrorotational (ROT) spectra with best fits derived from theoretical models. The difference in the DEP response of different capsule sizes can then be used as an efficient tool for separation of a specific capsule type from a heterogeneous population using a microfluidic platform. Such purification and collection of nematocyst sub‐populations is essential for further biochemical analysis.

No abstract