Parasitic cnidarians (Myxozoa) do not retain key oxygen-sensing and homeostasis tool-kit genes: Transcriptome assemblies

For aerobic organisms, both the Hypoxia-Inducible Factor (HIF) pathway and
the mitochondrial genomes are key players in regulating oxygen
homeostasis. However, recent work has suggested that these mechanisms are
not as highly conserved as previously thought, prompting more thorough
surveys across animal higher taxonomic levels, which would in turn permit
testing of hypotheses about the ecological conditions that may have
facilitated evolutionary loss of such genes. The phylum Cnidaria is known
to harbor wide variation in mitochondrial genome morphology, from typical
single circular chromosomes to fragmented linear chromosomes. More
recently, members of the cnidarian clade Myxozoa, comprising obligate
endoparasites, were shown to have lost their mitochondrial genome,
suggesting that variation in environmental oxygen availability may be a
key determinant in the evolution of metabolic gene networks. Here, we
surveyed genomes and transcriptomes across 42 cnidarian species for the
presence of HIF pathway members (HIFa, EGLN, VHL), as well as for an
assortment of hypoxia, mitochondrial, and stress-response toolkit genes.
We find that presence of the HIF pathway, as well as number of genes
associated with mitochondria, hypoxia, and stress response, do not vary
based on mitochondrial genome morphology. More interestingly, we uncover
evidence that myxozoans have lost the canonical HIF pathway repression
machinery, potentially altering HIF pathway functionality to work under
the specific conditions of their parasitic lifestyles. In addition,
relative to other cnidarians, myxozoans show loss of large proportions of
genes associated with the mitochondrion (~39%), and involved in response
to hypoxia (~27.5%) and general stress (~32%). Our results provide
additional evidence that the HIF regulatory machinery is evolutionarily
labile and that variations in the canonical system have evolved in many
animal groups.