One Ring does not rule them all: Linear mtDNA in Metazoa

Abstract

Recent advances in genome sequencing technologies have facilitated the exploration of the architecture of genomes, including mitochondrial genomes (mtDNA). In particular, whole genome sequencing has provided easier access to mitochondrial genomes with unusual organizations, which were difficult to obtain using traditional PCR-based approaches. As a consequence, there has been a steep increase in complete mtDNA sequences, particularly for Metazoa. The popular view of metazoan mtDNA is that of a small gene-dense circular chromosome. This view clashes with discoveries of a number of linear mtDNAs, particularly in non-bilaterian animals. Here, we review the distribution of linear mtDNA in Metazoa, namely in isopods, cnidarians, and sponges. We discuss the multiple origins of linear mitogenomes in these clades, where linearity has been linked to the likely insertion of a linear plasmid in cnidarians and the demosponge Acanthella acuta, while fixation of a heteroplasmy in the anticodon site of a tRNA might be responsible for the monolinear form of the mtDNA in some isopods. We also summarize our current knowledge of mechanisms that maintain the integrity of linear mitochromosomes, where a recurrent theme is the presence of terminal repeats that likely play the role of telomeres. We caution in defining a linear chromosome as complete, particularly when coding sequences and key features of linear DNA are missing. Finally, we encourage authors interested in mitogenome science to utilize all available data for linear mtDNA, including those tagged as “incomplete” or “unverified” in public databases, as they can still provide useful information such as phylogenetic characters and gene order.