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.2017 Aug 21;7(1):9010.
doi: 10.1038/s41598-017-09955-y.

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

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

Gadi Piriatinskiy et al. Sci Rep..

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.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1
Life cycle ofCeratonova shasta showing alternation between salmonid fish and polychaete worm hosts, infected by actinospore or myxospore, respectively. Myxospores have two polar capsules, and actinospores have three.
Figure 2
Figure 2
Isolation of polar capsules from whole myxospores. (a) IntactC. shasta myxospores with two polar capsules (P) and a binucleate sporoplasm (S). (b) Myxospores after valve cells (V) have been opened by SDS treatment, and polar capsules (P) stained dark with Toluidine blue. Note that polar capsules and valves are still held together with the spilled content of the spore. (c) Dissociated polar capsules and valves following enzymatic digestion. Scale bars = 5 μm.
Figure 3
Figure 3
DEP trapping and characterization of polar capsules. (a) Light microscope image of a mixture of capsules and valves within a quadrupole electrode array chip, used for DEP characterization, at 10Vpp and 2 MHz. Note that the capsules (yellow arrows) are trapped (i.e. pDEP) on the edge of the electrodes (E), whereas valves (white dashed circle and white arrowheads) are repelled (i.e. nDEP) from the electrodes. Scale bar = 100 μm. (b) Schematic description of the DEP-based microfluidic chip, which consists of a main channel with embedded electrode arrays. (c) A photo of the DEP-based chip, showing the sample loading (S), wash buffer (W) channels, and the collection reservoir (C). (d) Magnified view of the electrode array with trapped polar capsules. Inset (red box) shows magnified electrode and capsules. The entire separation process is shown in Supplementary Video 1.
Figure 4
Figure 4
Light microscope and SEM images of polar capsules and tubules. (a) Intact and activated polar capsules, pre-stained with Acridine orange. The arrow marks the florescence-stained tubule of the activated polar capsule; note that the activated capsules retain the dye. Bar = 5 μm. (b) SEM image of an unfired capsule. The operculum (arrow) is distinct. (c) Cryo-SEM image of the inverted, highly-packed tubule folded within an intact capsule. (d) Activated capsule with the everted tubule. (e) Released tubules with hooked ends (arrowed). Scale bars (b–e) 200 nm.
Figure 5
Figure 5
Main protein groups inC. shasta polar capsules identified by proteomic analysis. The polar capsule proteomic profile was divided to functional groups based on annotations and protein domain characterization and the percentage of each group from the 112 identified proteins is shown. For the full list, see Supplementary Table S1.
Figure 6
Figure 6
Comparison between capsule proteomic domains ofC. shasta and free-living cnidarians. (a) Venn diagram showing the number of InterPro (IPR) domains shared among the proteomes ofC. shasta,Hydra magnipapillata,Aurelia aurita andAnemonia virdis capsules. Identified domains for each organism are shown in the brackets. The highlighted sectors contain domains identified in all four organisms (yellow) or only in free-living cnidarians (orange). (b) Comparison of the percentages of IPR putative toxins and carbohydrate-related domains in the proteome ofC. shasta capsules and in the nematocysts of free-living cnidarians. For the full list of identified domains, see Supplementary Table S2.
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