Two Circular Chromosomes of Unequal Copy Number Make Up the Mitochondrial Genome of the Rotifer Brachionus plicatilis

Abstract

The monogonont rotifer Brachionus plicatilis is an emerging model system for a diverse array of questions in limnological ecosystem dynamics, the evolution of sexual recombination, cryptic speciation, and the phylogeny of basal metazoans. We sequenced the complete mitochondrial genome of B. plicatilis sensu strictu NH1L and found that it is composed of 2 circular chromosomes, designated mtDNA-I (11,153 bp) and mtDNA-II (12,672 bp). Hybridization to DNA isolated from mitochondria demonstrated that mtDNA-I is present at 4 times the copy number of mtDNA-II. The only nucleotide similarity between the 2 chromosomes is a 4.9-kbp region of 99.5% identity including a transfer RNA (tRNA) gene and an extensive noncoding region that contains putative D-loop and control sequence. The mtDNA-I chromosome encodes 4 proteins (ATP6, COB, NAD1, and NAD2), 13 tRNAs, and the large and small subunit ribosomal RNAs; mtDNA-II encodes 8 proteins (COX1-3, NAD3-6, and NAD4L) and 9 tRNAs. Gene order is not conserved between B. plicatilis and its closest relative with a sequenced mitochondrial genome, the acanthocephalan Leptorhynchoides thecatus, or other sequenced mitochondrial genomes. Polymerase chain reaction assays and Southern hybridization to DNA from 18 strains of Brachionus suggest that the 2-chromosome structure has been stable for millions of years. The novel organization of the B. plicatilis mitochondrial genome into 2 nearly equal chromosomes of 4-fold different copy number may provide insight into the evolution of metazoan mitochondria and the phylogenetics of rotifers and other basal animal phyla.

Genetic aspects of mitochondrial genome evolution

“…There is unequivocal evidence for recombination between different mini chromosomes, although the mechanism remains unknown (Shao and Barker, 2011). Multipartite mitogenomes have also been reported for the isopod Armadillidium vulgare (Raimond et al, 1999), the rotifer Brachionus plicatilis (Suga et al, 2008) and the nematode Globodera pallida (Armstrong et al, 2000).…”

“…In diploblasts, the deletion of many or even most tRNAs is a common phenomenon (Haen et al, 2010;Wang and Lavrov, 2008). Among protostomes, in particular Rotifera (Suga et al, 2008) and Onychophora (Braband et al, 2010) are affected. Marsupials are well known to have lost mt-tRNA-Lys (Dörner et al, 2001).…”

The massive mitochondrial genome of the angiosperm Silene noctiflora is evolving by gain or loss of entire chromosomes

“…Across eukaryotes, a variety of techniques have been used to identify and characterize multichromosomal mitochondrial genomes. As in this study, the identification of multichromosomal structures in angiosperms has been based almost exclusively on mapping/ sequencing (21-23), but, in some other cases, sequence data have been supplemented with electrophoretic separation of chromosomes and electron microscopy-based observations (11,12,14,15,17,18,20,45,46). To date, the only direct characterization of chromosomal structure in an angiosperm multichromosomal mitochondrial genome was performed in Silene vulgaris (26)(27)(28)(29)(30).…”

“…In contrast, mitochondrial genomes in many other eukaryotes have been radically transformed or even lost entirely. One recurring evolutionary pattern is the fragmentation of mitochondrial DNA (mtDNA) into multichromosomal genomes, which has occurred independently in a wide variety of taxa, including kinetoplastids (8), diplonemids (9), dinoflagellates (10), the green alga Polytomella parva (11), ichthyosporean protists (12), chytrid fungi (13), and multiple lineages of both metazoans (14)(15)(16)(17)(18)(19)(20) and angiosperms (21)(22)(23). The fragmentation of genomes into chromosomes is a very general property of eukaryotic nuclear genomes.…”

The expression pattern of dormancy-associated genes in multiple life-history stages in the rotifer Brachionus plicatilis

“…Relatively few molecular studies have been performed on B. plicatilis and most of them were limited to single gene or protein studies (Wheelock et al, 2002;Kaneko et al, 2002Kaneko et al, , 2005. Recently, sequencing of the mitochondrial DNA (Suga et al, 2008) and EST resources (Suga et al, 2007;Denekamp et al, 2009) became available. In a previous study (Denekamp et al, 2009), an attempt was made to identify biological processes associated with dormancy in rotifers.…”