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Linear Mitochondrial Genome in Anthozoa (Cnidaria): A Case Study in Ceriantharia.

ABSTRACT: Sequences and structural attributes of mitochondrial genomes have played a critical role in the clarification of relationships among Cnidaria, a key phylum of early-diverging animals. Among the major lineages of Cnidaria, Ceriantharia ("tube anemones") remains one of the most enigmatic in terms of its phylogenetic position. We sequenced the mitochondrial genomes of two ceriantharians to see whether the complete organellar genome would provide more support for the phylogenetic placement of Ceriantharia. For both Isarachnanthus nocturnus and Pachycerianthus magnus, the mitochondrial gene sequences could not be assembled into a single circular genome. Instead, our analyses suggest that both species have mitochondrial genomes consisting of multiple linear fragments. Linear mitogenomes are characteristic of members of Medusozoa, one of the major lineages of Cnidaria, but are unreported for Anthozoa, which includes the Ceriantharia. The inferred number of fragments and variation in gene order between species is much greater within Ceriantharia than among the lineages of Medusozoa. We identify origins of replication for each of the five putative chromosomes of the Isarachnanthus nocturnus mitogenome and for each of the eight putative chromosomes of the Pachycerianthus magnus mitogenome. At 80,923?bp, I. nocturnus now holds the record for the largest animal mitochondrial genome reported to date. The novelty of the mitogenomic structure in Ceriantharia highlights the distinctiveness of this lineage but, because it appears to be both unique to and diverse within Ceriantharia, it is uninformative about the phylogenetic position of Ceriantharia relative to other Anthozoa. The presence of tRNAMet and tRNATrp in both ceriantharian mitogenomes supports a closer relationship between Ceriantharia and Hexacorallia than between Ceriantharia and any other cnidarian lineage, but phylogenetic analysis of the genes contained in the mitogenomes suggests that Ceriantharia is sister to a clade containing Octocorallia?+?Hexacorallia indicating a possible suppression of tRNATrp in Octocorallia.

SUBMITTER: Stampar SN

PROVIDER: S-EPMC6465557 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Linear Mitochondrial Genome in Anthozoa (Cnidaria): A Case Study in Ceriantharia.

Stampar Sérgio N SN Broe Michael B MB Macrander Jason J Reitzel Adam M AM Brugler Mercer R MR Daly Marymegan M

Scientific reports 20190415 1

Sequences and structural attributes of mitochondrial genomes have played a critical role in the clarification of relationships among Cnidaria, a key phylum of early-diverging animals. Among the major lineages of Cnidaria, Ceriantharia ("tube anemones") remains one of the most enigmatic in terms of its phylogenetic position. We sequenced the mitochondrial genomes of two ceriantharians to see whether the complete organellar genome would provide more support for the phylogenetic placement of Cerian ...[more]

PMID: 30988357

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Project description:BackgroundLike all cnidarians, the subclass Ceriantharia (Cnidaria, Anthozoa) is known for producing cnidocysts, which mainly serve for prey immobilization, predator defense, and locomotion.AimThe present study aimed to understand the variability of the cnidom, i.e., the inventory of all cnidocyst types, in the ceriantharians (tube anemones) Ceriantheomorphe brasiliensis (10 individuals) and Cerianthus sp. (seven individuals).MethodsIn each individual, 30 intact cnidocysts of each identified type were measured in the following parts of tube anemones: marginal tentacles (four from each individual), labial tentacles (four from each individual), column, actinopharynx and metamesenteries. Each of these structures was divided into three levels (high, middle, and low) and the cnidom was analyzed. Statistical descriptive parameters (mean, standard deviation, minimum and maximum) of the sizes of all types of cnidocysts were calculated. The normality of the data for cnidocyst length was assessed using a Shapiro-Wilk test (α = 0.05). Based on the acceptance or rejection of the normality, either linear models or generalized linear models were used to evaluate variations in cnidocyst lengths. The normality of the cnidocyst length was tested by Shapiro-Wilk, and due to its rejection, generalized linear mixed models were applied to test the cnidocyst lengths variations.ResultsThe analysis of Ceriantheomorphe brasiliensis revealed 23 categories of cnidocysts, thereby expanding the understanding of its cnidome. The cnidoms of Ceriantheomorphe brasiliensis and Cerianthus sp. presented intraspecific variations, both qualitatively and in the lengths of cnidocysts. The cnidoms of the two species studied also showed qualitative intra-individual variations between different levels (high, middle, low) within each structure of the tube anemone (tentacles, actinopharynx, column and metamesenteries). Some cnidocyst types, such as atrichs from the column of C. brasiliensis, presented a length gradient along the column, from larger lengths at the "low" level to smaller lengths at the "high" level.ConclusionsThe cnidom of a tube anemone could be better described if samples are taken at different levels of the structures, as observed in C. brasiliensis. In addition, we can conclude that the cnidocyst lengths of both C. brasiliensis and Cerianthus sp. present intraspecific variation, which is coincident with that observed in actiniarian sea anemones. Moreover, as main conclusion, this work also proved that individuals of tube anemone species could present qualitative intra-structure variations in both the cnidom and cnidocyst lengths. This characteristic appears as an exception in cnidom variations, and has so far not been recorded even in the most studied actiniarian sea anemones. Finally, the intra-structure cnidocyst variations could reveal different functions of the different levels of a particular body part of the organisms.

Project description:BackgroundClassical morphological taxonomy places the approximately 1400 recognized species of Scleractinia (hard corals) into 27 families, but many aspects of coral evolution remain unclear despite the application of molecular phylogenetic methods. In part, this may be a consequence of such studies focusing on the reef-building (shallow water and zooxanthellate) Scleractinia, and largely ignoring the large number of deep-sea species. To better understand broad patterns of coral evolution, we generated molecular data for a broad and representative range of deep sea scleractinians collected off New Caledonia and Australia during the last decade, and conducted the most comprehensive molecular phylogenetic analysis to date of the order Scleractinia.MethodologyPartial (595 bp) sequences of the mitochondrial cytochrome oxidase subunit 1 (CO1) gene were determined for 65 deep-sea (azooxanthellate) scleractinians and 11 shallow-water species. These new data were aligned with 158 published sequences, generating a 234 taxon dataset representing 25 of the 27 currently recognized scleractinian families.Principal findings/conclusionsThere was a striking discrepancy between the taxonomic validity of coral families consisting predominantly of deep-sea or shallow-water species. Most families composed predominantly of deep-sea azooxanthellate species were monophyletic in both maximum likelihood and Bayesian analyses but, by contrast (and consistent with previous studies), most families composed predominantly of shallow-water zooxanthellate taxa were polyphyletic, although Acroporidae, Poritidae, Pocilloporidae, and Fungiidae were exceptions to this general pattern. One factor contributing to this inconsistency may be the greater environmental stability of deep-sea environments, effectively removing taxonomic "noise" contributed by phenotypic plasticity. Our phylogenetic analyses imply that the most basal extant scleractinians are azooxanthellate solitary corals from deep-water, their divergence predating that of the robust and complex corals. Deep-sea corals are likely to be critical to understanding anthozoan evolution and the origins of the Scleractinia.

Dataset Information

Linear Mitochondrial Genome in Anthozoa (Cnidaria): A Case Study in Ceriantharia.

Publications

Linear Mitochondrial Genome in Anthozoa (Cnidaria): A Case Study in Ceriantharia.

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