Ceratonova shasta: a cnidarian parasite of annelids and salmonids

Abstract

The myxozoan Ceratonova shasta was described from hatchery rainbow trout over 70 years ago. The parasite continues to cause severe disease in salmon and trout, and is recognized as a barrier to salmon recovery in some rivers. This review incorporates changes in our knowledge of the parasite's life cycle, taxonomy and biology and examines how this information has expanded our understanding of the interactions between C. shasta and its salmonid and annelid hosts, and how overarching environmental factors affect this host–parasite system. Development of molecular diagnostic techniques has allowed discrimination of differences in parasite genotypes, which have differing host affinities, and enabled the measurement of the spatio-temporal abundance of these different genotypes. Establishment of the C. shasta life cycle in the laboratory has enabled studies on host–parasite interactions and the availability of transcriptomic data has informed our understanding of parasite virulence factors and host defences. Together, these advances have informed the development of models and management actions to mitigate disease.

Keywords: Actinospore; Myxozoa; disease; enteronecrosis; environmental factors; epidemiology; fish immunity; intra-specific parasite diversity; management; monitoring; myxospore.

Graphical abstract

Fig. 1.

The complex life cycle of Ceratonova shasta involves 2 spore stages and 2 obligate hosts: a salmonid fish and the annelid Manayunkia occidentalis. Clockwise from left: waterborne actinospores (A) sense the fish and discharge their nematocysts (B). The parasite sporoplasm penetrates the gill epithelium (C) where it begins to proliferate (D), then enters the host bloodstream (E). The parasite travels to the intestine, migrates between tissue layers (F), further proliferates and then sporulates (G). Mature myxospores (H) are released with feces or from the decomposed carcass. Waterborne myxospores encounter the annelid host, discharge their nematocysts (I) and penetrate the annelid intestine. The parasite migrates to the body wall where it proliferates (J, K), then sporulates into actinospores (L, M), which burst from the body wall (N). Scale: black bar = 10 μm, hollow bar = 100 μm.

Fig. 2.

Multipartite components of enteronecrosis.

Fig. 3.

Ceratonova shasta genotypes and their distinguishing characters. Sympatric/allopatric designators are used to characterize stocks with origins from waters with or without C. shasta, respectively. Histological sections of the intestine stained with H&E; O and II = allopatric rainbow trout, I = Chinook salmon. [1] Atkinson and Bartholomew (2010b); [2] Stinson et al. (2018); [3] Stinson and Bartholomew (2012); [4] Hurst et al. (2012).

Fig. 4.

Ceratonova shasta cell protrusions. (A) Developmental stages, 2 of them showing abundant static filopodia; (B) Parasite stages with lamellipodia and small filopodia projecting in the external margin; (C) 3D radiating pattern of filopodia; (D) active blebbing parasite stages with 5 overlapping blebs (white arrowheads); (E) external appearance of 2 blebs; (F) stage with profuse blebbing at the anterior end and a posterior end with extensible filaments that anchored the stage to other cells. A–E: genotype IIR, rainbow trout ascites; F: genotype I, Chinook salmon ascites; A, D, F: light microscopy; B–C, E: scanning electron microscopy.

Fig. 5.

Annelid host of Ceratonova shasta. (A) Collection by SCUBA; (B) annelid tubes at low density anchored in encrusting periphyton; (C) annelid tubes at high density; (D) annelids feeding from their tubes; (E) mature annelid, bar 1 mm (authors' images).

Fig. 6.

Possible management actions and goals to affect each phase of the Ceratonova shasta life cycle, targeting both hosts and the parasite directly. *Intestines removed from carcasses before out-planting.