Abstract
Two major transitions in animal evolution–the origins of multicellularity and bilaterality–correlate with major changes in mitochondrial DNA (mtDNA) organization. Demosponges, the largest class in the phylum Porifera, underwent only the first of these transitions and their mitochondrial genomes display a peculiar combination of ancestral and animal-specific features. To get an insight into the evolution of mitochondrial genomes within the Demospongiae, we determined 17 new mtDNA sequences from this group and analyzing them with five previously published sequences. Our analysis revealed that all demosponge mtDNAs are 16- to 25-kbp circular molecules, containing 13–15 protein genes, 2 rRNA genes, and 2–27 tRNA genes. All but four pairs of sampled genomes had unique gene orders, with the number of shared gene boundaries ranging from 1 to 41. Although most demosponge species displayed low rates of mitochondrial sequence evolution, a significant acceleration in evolutionary rates occurred in the G1 group (orders Dendroceratida, Dictyoceratida, and Verticillitida). Large variation in mtDNA organization was also observed within the G0 group (order Homosclerophorida) including gene rearrangements, loss of tRNA genes, and the presence of two introns in Plakortis angulospiculatus. While introns are rare in modern-day demosponge mtDNA, we inferred that at least one intron was present in cox1 of the common ancestor of all demosponges. Our study uncovered an extensive mitochondrial genomic diversity within the Demospongiae. Although all sampled mitochondrial genomes retained some ancestral features, including a minimally modified genetic code, conserved structures of tRNA genes, and presence of multiple non-coding regions, they vary considerably in their size, gene content, gene order, and the rates of sequence evolution. Some of the changes in demosponge mtDNA, such as the loss of tRNA genes and the appearance of hairpin-containing repetitive elements, occurred in parallel in several lineages and suggest general trends in demosponge mtDNA evolution.
Highlights
Two major evolutionary events occurred early in animal history and shaped the majority of animals, as we know them today: the origin of multicellularity and the origin of bilateral symmetry
24 or 25 tRNA genes were present in most analyzed demosponge mitochondrial genomes, as few as 2 and as many as 27 tRNA genes were found in mitochondrial genomes of some demosponge species (Figure 2, see below)
Among the features shared among all sampled demosponge mitochondrial genomes are compact organization of the genetic material, similar gene content, well conserved structures of encoded tRNAs, a minimally modified genetic code for mitochondrial translation, and the absence of a single large ‘‘control’’ region characteristic of mitochondrial DNA (mtDNA) in bilaterian animals
Summary
Two major evolutionary events occurred early in animal history and shaped the majority of animals, as we know them today: the origin of multicellularity and the origin of bilateral symmetry. The origin of bilaterality correlates with further compaction of mtDNA, multiple changes in the genetic code and the associated losses of some tRNA genes, along with the appearance of several genetic novelties [4]. The picture presented above is an extrapolation of our knowledge of extant organisms into the ancient past and as such can be affected by artifacts of ancestral state reconstruction [5]. It is based on a relatively limited sampling of mitochondrial genomes, especially from non-bilaterian animals, and additional data from Cnidaria, Ctenophora, Porifera, as well as the closely related lineages of eukaryotes (e.g., Choanozoa) are essential to support, expand, or refute it
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