The Molecular Mechanisms Employed by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) from Invasion through Sporulation for Successful Proliferation in Its Fish Host

Author:

Maor-Landaw Keren1,Avidor Itamar1,Rostowsky Nadav1,Salti Barbara1,Smirnov Margarita2ORCID,Ofek-Lalzar Maya3,Levin Liron4,Brekhman Vera1,Lotan Tamar1ORCID

Affiliation:

1. Marine Biology Department, The Leon H. Charney School of Marine Sciences, University of Haifa, Mt. Carmel, Haifa 3103301, Israel

2. Central Fish Health Laboratory, Department of Fisheries and Aquaculture, Ministry of Agriculture and Rural Development, Nir David 1080300, Israel

3. Bioinformatic Unit, University of Haifa, Mt. Carmel, Haifa 3498838, Israel

4. Bioinformatics Core Facility, llse Katz Institute for Nanoscale Science and Technology, Ben-Gurion University of the Negev, Beer-Sheva 8410501, Israel

Abstract

Myxozoa is a unique group of obligate endoparasites in the phylum Cnidaria that can cause emerging diseases in wild and cultured fish populations. Recently, we identified a new myxozoan species, Myxobolus bejeranoi, which infects the gills of cultured tilapia while suppressing host immunity. To uncover the molecular mechanisms underlying this successful parasitic strategy, we conducted transcriptomics analysis of M. bejeranoi throughout the infection. Our results show that histones, which are essential for accelerated cell division, are highly expressed even one day after invasion. As the infection progressed, conserved parasitic genes that are known to modulate the host immune reaction in different parasitic taxa were upregulated. These genes included energy-related glycolytic enzymes, as well as calreticulin, proteases, and miRNA biogenesis proteins. Interestingly, myxozoan calreticulin formed a distinct phylogenetic clade apart from other cnidarians, suggesting a possible function in parasite pathogenesis. Sporogenesis was in its final stages 20 days post-exposure, as spore-specific markers were highly expressed. Lastly, we provide the first catalog of transcription factors in a Myxozoa species, which is minimized compared to free-living cnidarians and is dominated by homeodomain types. Overall, these molecular insights into myxozoan infection support the concept that parasitic strategies are a result of convergent evolution.

Funder

Israel Science Foundation

University of Haifa

Publisher

MDPI AG

Subject

Inorganic Chemistry,Organic Chemistry,Physical and Theoretical Chemistry,Computer Science Applications,Spectroscopy,Molecular Biology,General Medicine,Catalysis

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