Unique mitochondrial genome architecture in unicellular relatives of animals

Abstract

Animal mtDNAs are typically small (approximately 16 kbp), circular-mapping molecules that encode 37 or fewer tightly packed genes. Here we investigate whether similarly compact mitochondrial genomes are also present in the closest unicellular relatives of animals, i.e., choanoflagellate and ichthyosporean protists. We find that the gene content and architecture of the mitochondrial genomes of the choanoflagellate Monosiga brevicollis, the ichthyosporean Amoebidium parasiticum, and Metazoa are radically different from one another. The circular-mapping choanoflagellate mtDNA with its long intergenic regions is four times as large and contains two times as many protein genes as do animal mtDNAs, whereas the ichthyosporean mitochondrial genome totals >200 kbp and consists of several hundred linear chromosomes that share elaborate terminal-specific sequence patterns. The highly peculiar organization of the ichthyosporean mtDNA raises questions about the mechanism of mitochondrial genome replication and chromosome segregation during cell division in this organism. Considering that the closest unicellular relatives of animals possess large, spacious, gene-rich mtDNAs, we posit that the distinct compaction characteristic of metazoan mitochondrial genomes occurred simultaneously with the emergence of a multicellular body plan in the animal lineage.

Figure 1

Genetic map of M. brevicollis mtDNA. Exons are depicted by black boxes, group I introns by open boxes, and intronic ORFs (coding for potential endonucleases) by shaded boxes. All genes are transcribed in a clockwise direction. Black labels denote genes common to animal and fungal mtDNAs, blue labels represent genes typically not found in either animal or fungal mtDNAs, and green labels denote unique ORFs of unknown function.

Figure 2

Mitochondrial chromosomes of A. parasiticum, separated by agarose gel electrophoresis. Lane a, mtDNA fraction, as isolated. Lane b, A 1-kbp ladder (Stratagene) included as a size marker.

Figure 3

Structure and genetic maps of three representative mitochondrial chromosomes of A. parasiticum. Genes, introns, and ORFs are represented by boxes, as in Fig. 1. Terminal repeat motifs are represented by a blue triangle (repx), a yellow lozenge (repa), and a red octagon (repb), and internal repeat motifs by blue rectangles. The numerals denote different internal repeat motifs. Depicted chromosomes have the following identifiers and GenBank accession nos.: (a) 0316riay49 (AF538050); (b) 2902riaz91 (AF538047); and (c) 2153iay75 (AF538045). (d) Sequence of the terminal repeats of chromosome 0316riay49 (GenBank accession no. AF538050). The background colors blue, yellow, and red correspond to repx, repa, and repb, respectively.