Linear Mitochondrial genome in Anthozoa (Cnidaria): A case study in Ceriantharia

Abstract

Sequences and structural attributes of mitochondrial genomes have played a key 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 groups 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 ceriantharian species studied, the mitochondrial gene sequences could not be assembled into a circular genome. Instead, our analyses suggest both species have fragmented 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 number of fragments and the variation in gene order between species is much greater in Ceriantharia than among Medusozoa. 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 anthozoan groups.

Transcriptomic Analysis of Four Cerianthid (Cnidaria, Ceriantharia) Venoms

“…Their phylogenetic placement within Cnidaria remains contentious, due to a combination of a lack of available sequence data and low species sampling [ 5 , 67 , 68 ]. Various studies place them as sister group to Hexacorallia, sister group to Octocorallia [ 69 ], or sister group to Hexacorallia + Octocorallia (i.e., sister to all other anthozoans) [ 70 , 71 ]. Although cerianthids are clearly members of Anthozoa, they have several features that are more similar to Medusozoa.…”

“…Although cerianthids are clearly members of Anthozoa, they have several features that are more similar to Medusozoa. For instance, cerianthids possess linear mitochondrial genomes, as in medusozoans, while all other anthozoans have circular mitochondrial genomes [ 71 , 72 , 73 ]. Also, unlike other anthozoans, cerianthids display a long-lived pelagic larval stage that superficially resembles a medusa [ 74 ].…”

Extensive gene rearrangements in the mitogenomes of congeneric annelid species and insights on the evolutionary history of the genus Ophryotrocha

“…Maternal inheritance and near absence of recombination have popularised its use in many eukaryotes [ 3 ]. Most of metazoan mitochondrial genomes are circular molecules that typically include 13 protein coding genes (PCG), two ribosomal RNA genes, 22 transfer RNA genes and a control region ([ 4 ], but see [ 5 , 6 ]). The mitochondrial gene content is almost invariant among species, but the gene order has been found to vary considerably across Metazoans (such as flatworms, molluscs and tunicates [ 7 ]), generating interest in using mitochondrial DNA (mtDNA) gene order for phylogenetic inference [ 2 ].…”

Evolutionary implications of analyses of complete mitochondrial genomes across order Zoantharia (Cnidaria: Hexacorallia)

“…Analyses of complete mitochondrial genomes (mt‐genome) have been used to infer phylogenetic relationships and help clarify the complex evolution of early‐diverging animals (Bridge, Cunningham, Schierwater, DeSalle, & Buss, 1992; Lavrov & Pett, 2016). Cnidarians of the class Anthozoa generally have circular mt‐genomes (Bridge, Cunningham, DeSalle, & Buss, 1995; Emblem et al, 2014; Lin et al, 2014; Medina, Collins, Takaoka, Kuehl, & Boore, 2006), although subclass Ceriantharia has recently been shown to have fragmented linear mitogenomes (Stampar et al, 2019). Molecular phylogenetic reconstructions using complete mt‐genomes have been performed for several orders of Anthozoa, including corallimorpharians (order Corallimorpharia), hard corals (order Scleractinia), and sea anemones (order Actiniaria) (Chuang & Chen, 2017; Emblem et al, 2014; Foox, Brugler, Siddall, & Rodríguez, 2016; Lin et al, 2016; Medina et al, 2006), but such analyses have not been conducted for zoantharians (order Zoantharia).…”