Abstract

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.

Highlights

  • Myxozoa is a diverse, speciose group of microscopic parasites, recently placed within the phylum Cnidaria

  • In comparison to the thousands to millions of capsules found in free-living cnidarians, the C. shasta myxospore contains only two polar capsules (r = 0.9 μm), which are tightly embedded within two valves (Fig. 2a), considerably limiting the availability of study materials

  • At 5 MHz, the valves were repelled from the field maxima at the electrode edge (i.e. experiencing negative dielectric properties (DEP)), whereas the capsules were strongly attracted to the edge as a result of positive DEP (Fig. 3a)

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Summary

Introduction

Speciose group of microscopic parasites, recently placed within the phylum Cnidaria. 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. 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. The nematocyst of free-living cnidarians is likely the most evolutionarily ancient venom delivery apparatus in extant multicellular organisms. These organelles are present in large numbers and operate as a micro-weaponry system capable of entangling and penetrating prey or predator, and injecting toxins at an ultrafast acceleration of more than 5 million g16–18. Identification of genes that are expressed in these capsules would facilitate better understanding of myxozoan evolutionary adaptations to parasitism

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