Acanthella acuta Mitochondrial DNA: Linear Architecture and Other Unique Features

While Acanthella acuta (Schmidt 1862), a common demosponge found in the Mediterranean Sea and Atlantic Ocean, is -- morphologically -- little distinguishable from other sponges, its mitochondrial DNA (mtDNA) is unique within the class. In contrast to all other studied demosponges, A. acuta mtDNA appears to be linear and displays several unusual features: inverted terminal repeats, group II introns in three mt-genes, and two unique ORFs. One of the ORFs (ORF1535) combines a DNA-polymerase domain with a DNA-directed RNA-polymerase domain, while the second bears no discernable similarity to any reported sequences. The group II intron within the cox2 gene is the first such intron reported in an animal. Our phylogenetic analyses indicate that the cox1 intron is related to similar introns found in other demosponges, while the cox2 intron is likely not of animal origin. The two domains found within ORF1535 do not share a common origin and, along with the cox2 intron, were likely acquired by horizontal transfer. The findings of this paper open new avenues of exploration in the understanding of mtDNA linearization within Metazoa. SignificanceThe transition from circular to linear mtDNA architecture is a rare and poorly understood phenomenon in animals. In addition, the few lineages that made this transition (Medusozoa, Calcarea, and Isopoda), adopted linear mt-DNA architecture early in their history, making it difficult to reconstruct the underlying events. The identification of linear mtDNA in Acanthella acuta not only provides an independent example of the origin of linear mtDNA architectures in animals but also an opportunity to investigate its evolution at a much shorter evolutionary time. In particular, the conservation of circular mtDNA in other studied species within the family Dictyonellidae highlights the need to investigate other species in the genus Acanthella, to better understand mtDNA linearization in A. acuta.