A fragmented metazoan organellar genome: the two mitochondrial chromosomes of Hydra magnipapillata

Abstract Background Animal mitochondrial (mt) genomes are characteristically circular molecules of ~16–20 kb. Medusozoa (Cnidaria excluding Anthozoa) are exceptional in that their mt genomes are linear and sometimes subdivided into two to presumably four different molecules. In the genus Hydra, the mt genome comprises one or two mt chromosomes. Here, we present the whole mt genome sequence from the hydrozoan Hydra magnipapillata, comprising the first sequence of a fragmented metazoan mt genome encoded on two linear mt chromosomes (mt1 and mt2). Results The H. magnipapillata mt chromosomes contain the typical metazoan set of 13 genes for respiratory proteins, the two rRNA genes and two tRNA genes. All genes are unidirectionally oriented on mt1 and mt2, and several genes overlap. The gene arrangement suggests that the two mt chromosomes originated from one linear molecule that separated between nd5 and rns. Strong correlations between the AT content of rRNA genes (rns and rnl) and the AT content of protein-coding genes among 24 cnidarian genomes imply that base composition is mainly determined by mt genome-wide constraints. We show that identical inverted terminal repeats (ITR) occur on both chromosomes; these ITR contain a partial copy or part of the 3' end of cox1 (54 bp). Additionally, both mt chromosomes possess identical oriented sequences (IOS) at the 5' and 3' ends (5' and 3' IOS) adjacent to the ITR. The 5' IOS contains trnM and non-coding sequences (119 bp), whereas the 3' IOS comprises a larger part (mt2) with a larger partial copy of cox1 (243 bp). Conclusion ITR are also documented in the two other available medusozoan mt genomes (Aurelia aurita and Hydra oligactis). In H. magnipapillata, the arrangement of ITR and 5' IOS and 3' IOS suggest that these regions are crucial for mt DNA replication and/or transcription initiation. An analogous organization occurs in a highly fragmented ichthyosporean mt genome. With our data, we can reject a model of mt replication that has previously been proposed for Hydra. This raises new questions regarding replication mechanisms probably employed by all medusozoans, and also has general implications for the expected organization of fragmented linear mt chromosomes of other taxa.