A fragmented metazoan organellar genome: the two mitochondrial chromosomes of Hydra magnipapillata - PubMed (original) (raw)

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

Oliver Voigt et al. BMC Genomics. 2008.

Abstract

Background: Animal mitochondrial (mt) genomes are characteristically circular molecules of approximately 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.

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Figures

Figure 1

Figure 1

Organization of the H. magnipapillata mt chromosomes (mt1 and mt2). A: In comparison to the linear mt genome of H. oligactis (Hydrozoa) and Aurelia aurita (Scyphozoa), drawn to scale. Arrows indicate orientation of genes in Aurelia. Numbered black bars above H. magnipapillata mt chromosomes correspond to the PCR fragments amplified from Hydra sp. (Additional file 3). Arrows in grey indicate the proposed duplications of terminal sequences in the mt chromosome separation process. B: Organization at the 5' and 3' ends of mt1 and mt2 in H. magnipapillata. Arrows in the inverted terminal repeats (ITR) are drawn according to the orientation of the cox1 fragment. C: Alignment of the ends of the ITR from H. oligactis, H. vulgaris (mt1) and H. magnipapillata (mt1 and mt2). * = sequence displayed as reverse complement.

Figure 2

Figure 2

Base composition in cnidarian mt genomes. Correlations of AT content (%) of mt rRNAs and the AT content (%) in the codon positions 1, 2 and 3 calculated from 13 protein-coding genes of 24 cnidarian mt genomes (Additional file 4). Black filled symbols = H. magnipapillata; grey filled symbols = H. oligactis.

Figure 3

Figure 3

Evolution of cnidarian mt organization. A. Summary of relationships of higher cnidarian taxa according to nc Small and Large Subunit rRNA data [37], and the organization of mt genomes. Note that in [15] only the size of mt chromosome carrying rnl was examined. B. Summary of relationships within the genus Hydra based upon our ML and Bayesian analyses of partial cox1 data, rooted with other hydrozoan sequences from GenBank (accession numbers are given after each species name). Support values >50 are shown above branches (ML bootstraps/Bayesian posterior probability, * = 100 in both analyses). Sequences from this study are bold. Expected mt genome organization is shown in grey. 1syn.: Hydra viridis; H. viridissima.

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