A myxozoan genome reveals mosaic evolution in a parasitic cnidarian

Abstract

Background Parasite evolution has been conceptualized as a process of genetic loss and simplification. Contrary to this model, there is evidence of expansion and conservation of gene families related to essential functions of parasitism in some parasite genomes, reminiscent of widespread mosaic evolution—where subregions of a genome have different rates of evolutionary change. We found evidence of mosaic genome evolution in the cnidarian Myxobolus honghuensis, a myxozoan parasite of fish, with extremely simple morphology. Results We compared M. honghuensis with other myxozoans and free-living cnidarians, and determined that it has a relatively larger myxozoan genome (206 Mb), which is less reduced and less compact due to gene retention, large introns, transposon insertion, but not polyploidy. Relative to other metazoans, the M. honghuensis genome is depleted of neural genes and has only the simplest animal immune components. Conversely, it has relatively more genes involved in stress resistance, tissue invasion, energy metabolism, and cellular processes compared to other myxozoans and free-living cnidarians. We postulate that the expansion of these gene families is the result of evolutionary adaptations to endoparasitism. M. honghuensis retains genes found in free-living Cnidaria, including a reduced nervous system, myogenic components, ANTP class Homeobox genes, and components of the Wnt and Hedgehog pathways. Conclusions Our analyses suggest that the M. honghuensis genome evolved as a mosaic of conservative, divergent, depleted, and enhanced genes and pathways. These findings illustrate that myxozoans are not as genetically simple as previously regarded, and the evolution of some myxozoans is driven by both genomic streamlining and expansion.

Genome-Scale Analysis Reveals Extensive Diversification of Voltage-Gated K+ Channels in Stem Cnidarians

“…The inclusion of two schyphozoans ( Rhopilema esculentum , flame jellyfish; Sanderia malayensis , pelagic jellyfish) and a hydrozoan ( H. vulgaris , freshwater hydra) provided us with insight into channel ancestry and diversification within the medusozoan lineage. We did not include Endocnidozoa in our study because they derive from the same common ancestor as Anthozoa and Hydrozoa ( Kayal et al 2018 ) and have undergone extensive neuronal gene loss ( Guo et al 2022 ). We therefore reasoned that they would provide limited insight into the voltage-gated K + channel set of stem cnidarians.…”

Transcriptomic Insights into the Diversity and Evolution of Myxozoa (Cnidaria, Endocnidozoa) Toxin-like Proteins

“…Our analysis was mainly based on transcriptomes, but we also added five genomes ( M. squamalis , T. kitauei , H. salminicola , K. iwatai , and M. honghuensis [ 23 , 30 , 31 ]) to the project to detect the extent of trait differences. When comparing the results of genomic and transcriptomic analyses, we found that most of the species had more TLPs in the transcriptomes, such as M. squamalis (11 vs. 9), M. honghuensis (19 vs. 12), T. kitauei (20 vs. 10), and H. salminicola (9 vs. 8).…”

The highly repetitive genome of Myxobolus sp., a myxozoan parasite of fathead minnows

“…In this study, we set out to sequence, assemble, and annotate the genome of M. rasmusseni . This is only the second time that long-read sequencing technology has been used for the myxozoans, the first being Myxobolus honghuensis (Guo et al, 2022). The assembled genome is the largest of any myxozoan sequenced to date.…”