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

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.

A genome wide survey reveals multiple nematocyst-specific genes in Myxozoa

“…However, it is worth noting that the soluble content of the Hydra nematocyst is known to contain ~ 300 proteins [ 13 ] while the shell proteome represents only ~ 100 proteins, including ~ 20 minicollagen genes [ 14 ]. In agreement, the polar capsule proteome of C. shasta is expected to represent mainly shell proteins since C. shasta polar capsules are incapable of injection and do not contain venom proteins [ 17 ].These numbers suggest that the nematocysts shell is composed of about a hundred proteins, among which only minicollagens and nematogalectins have been recognized as core proteins shared by all cnidarian lineages.…”

“…Thus far, the entire nematocyst proteome, which also include collagenous proteins which form the nematocyst shell, has only been characterized for H. vulgaris [ 14 ] and recently for the myxozoan Ceratonova shasta [ 17 ]. These two studies revealed a difference in protein numbers, with 410 unique proteins in Hydra and only 112 in Ceratonova.…”

“…Previous investigations have identified a number of cnidarian-restricted, nematocyst-specific genes and proteins [ 13 – 17 ]. In this study, we aimed to determine whether myxozoans possess nematocyst-specific proteins (other than nematogalectins and minicollagens, which have been characterized in Myxozoa in several works [ 6 , 11 , 15 , 17 – 19 ]) to better understand the origins and evolution of myxozoan polar capsules from cnidarian nematocysts. Using a database of nematocyst-specific proteins generated through a Hydra nematocyst proteome sequencing [ 14 ], we searched myxozoan and other cnidarian genomic and transcriptomic databases for proteins with similar sequences.…”

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

“…The staining intensity and consistency across the myxozoans examined with these stains suggest a highly acidic, electron‐dense environment within the polar capsules. This may reflect the presence of poly‐gamma‐glutamate, a polymer composed of an electron‐dense matrix that binds cations present in the nematocysts of Cnidarians and potentially the polar capsules of C. shasta (Piriatinskiy et al, 2017; Szczepanek, Cikala, & David, 2002; Weber, 1990).…”

Comparative transcriptomics and host-specific parasite gene expression profiles inform on drivers of proliferative kidney disease

“…Minicollagens are likely to play a similar role to those in free-living cnidarians providing the high tensile strength needed to facilitate polar filament deployment 59 . In myxozoans this enables spores to attach to hosts.…”