Abstract
BackgroundThe animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria. Extant members from this phylum, therefore, are important resources for understanding the evolution of the nervous system. Cnidarian nervous systems are strongly peptidergic. Using genomics, we have recently shown that three neuropeptide families (the X1PRX2amides, GRFamides, and GLWamides) are wide-spread in four (Scyphozoa, Cubozoa, Staurozoa, Anthozoa) out of six cnidarian classes or subphyla, suggesting that these three neuropeptide families emerged in the common cnidarian ancestor. In the current paper, we analyze the remaining cnidarian class, Hydrozoa, and the subphylum Endocnidozoa, to make firm conclusions about the evolution of neuropeptide genes in Cnidaria.ResultsWe analyzed sixteen hydrozoan species with a sequenced genome or transcriptome, using a recently developed software program for discovering neuropeptide genes. These species belonged to various hydrozoan subclasses and orders, among them the laboratory models Hydra, Hydractinia, and Clytia. We found that each species contained three to five neuropeptide families. A common feature for all hydrozoans was that they contained genes coding for (i) X1PRX2amide peptides, (ii) GRFamide peptides, and (iii) GLWamide peptides. These results support our previous conclusions that these three neuropeptide families evolved early in evolution. In addition to these three neuropeptide families, hydrozoans expressed up to two other neuropeptide gene families, which, however, were only occurring in certain animal groups. Endocnidozoa (Myxozoa) are microscopically small endoparasites, which are strongly reduced. For long, it was unknown to which phylum these parasites belonged, but recently they have been associated with cnidarians. We analyzed nine endocnidozoan species and found that two of them (Polypodium hydriforme and Buddenbrockia plumatellae) expressed neuropeptide genes. These genes coded for neuropeptides belonging to the GRFamide and GLWamide families with structures closely resembling them from hydrozoans.ConclusionsWe found X1PRX2amide, GRFamide, and GLWamide peptides in all species belonging to the Hydrozoa, confirming that these peptides originated in the common cnidarian ancestor. In addition, we discovered GRFamide and GLWamide peptide genes in some members of the Endocnidozoa, thereby linking these parasites to Hydrozoa.
Highlights
The animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa
The anatomy of the cnidarian nervous system can be best described as a nerve net that on some locations has condensed to form nervous plexuses, or giant nerves [11,12,13,14,15,16,17,18]. For long it had been a mystery, which neurotransmitters were used by the cnidarian nervous systems, but in the eighties, we discovered that cnidarian nervous systems were peptidergic
After having analyzed five cubozoan species, four scyphozoan species, six staurozoan species, seven species belonging to the Octocorallia, nineteen species belonging to Hexacorallia, and one Ceriantharia species – analyzing altogether 80 genome or transcriptome databases - we found that three neuropeptide families turned out to be wide-spread in Cnidaria: The X1PRX2amide, GRFamide, and GLWamide families [52, 53]
Summary
The animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria Extant members from this phylum, are important resources for understanding the evolution of the nervous system. About 700–800 million years ago, four phyla diverged from the main evolutionary lineage of animals that led to the Bilateria [1, 2] These four animal phyla were Porifera (sponges), Ctenophora (comb jellyfishes), Placozoa (1-mm small, disk-like animals), and Cnidaria (animals like sea anemones, corals and jellyfishes). Extant members of Porifera, Ctenophora, Placozoa, and Cnidaria, are invaluable resources for identifying ancestral building blocks needed for the functioning of the nervous and endocrine systems and many other processes important for multicellular animals. The neurotransmitters in Ctenophora have not been identified yet, but both the endocrine systems in Placozoa [8,9,10] and the nervous systems in Cnidaria [6, 7] use neuropeptides for signal transmission, suggesting that neuropeptides must have played central roles in the evolution of early neuroendocrine systems
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