Evolution of Extensively Fragmented Mitochondrial Genomes in the Lice of Humans

Abstract

Bilateral animals are featured by an extremely compact mitochondrial (mt) genome with 37 genes on a single circular chromosome. The human body louse, Pediculus humanus, however, has its mt genes on 20 minichromosomes. We sequenced the mt genomes of two other human lice: the head louse, P. capitis, and the pubic louse, Pthirus pubis. Comparison among the three human lice revealed the presence of fragmented mt genomes in their most recent common ancestor, which lived ∼7 Ma. The head louse has exactly the same set of mt minichromosomes as the body louse, indicating that the number of minichromosomes, and the gene content and gene arrangement in each minichromosome have remained unchanged since the body louse evolved from the head louse ∼107,000 years ago. The pubic louse has the same pattern of one protein-coding or rRNA gene per minichromosome (except one minichromosome with two protein-coding genes, atp6 and atp8) as the head louse and the body louse. This pattern is apparently ancestral to all human lice and has been stable for at least 7 Myr. Most tRNA genes of the pubic louse, however, are on different minichromosomes when compared with their counterparts in the head louse and the body louse. It is evident that rearrangement of four tRNA genes (for leucine, arginine and glycine) was due to gene-identity switch by point mutation at the third anticodon position or by homologous recombination, whereas rearrangement of other tRNA genes was by gene translocation between minichromosomes, likely caused by minichromosome split via gene degeneration and deletion.

Variation in mitochondrial minichromosome composition between blood-sucking lice of the genus Haematopinus that infest horses and pigs

“…Ten pairs of mitochondrial genes share stretches of identical sequences longer than expected by chance in the blood-sucking lice of humans and pigs, providing unequivocal evidence for DNA recombination between mt genes and between minichromosomes in these lice [14,16]. We found that nine pairs of mt genes in the horse louse, H. asini , also share stretches of identical sequences longer than expected by chance (Table 2).…”

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

“…Sometimes the levels of fragmentation are minor: the mtDNA of the colorless green alga Polytomella piriformis is divided into two small (<15 kb) linear chromosomes (44). In other instances, the fragmentation is extensive: human head louse mtDNA is broken into 20 miniature (1.5-3 kb) circular chromosomes, each encoding one to three genes (50), and the euglenozoan Diplonema papillatum mtDNA comprises >75 small (6-7 kb) circular DNAs with single-gene modules (51). Trypanosome mtDNAs form giant, intertwined networks (kinetoplasts) comprising thousands of small (0.5-10 kb) and a few dozen large (20-40 kb) circular chromosomes (52), and the Amoebidium parasiticum mtDNA is made up of hundreds of 0.3-to 8.3-kb linear pieces (53).…”

“…Nevertheless, the oversampling of mitochondrial genomes within some clades has contributed to the range of observed organelle genome diversity. For example, an excess of arthropod mitochondrial genome sequencing resulted in the discovery of the abnormal mtDNAs from lice (50). There are, of course, many eukaryotic lineages that harbor mitochondria but not plastids, so even if plastids genomes are well sampled in the lineages that contain plastids, there are still more mitochondrial lineages to sample (52).…”

Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications

“…The most common type of rearrangement involves the tRNA genes, among which the gene orders in Hymenoptera, Thysanoptera, Psocoptera and Phthiraptera exhibit more frequent rearrangements compared with the putative ancestral gene order (Shao and Barker, 2003;Shao et al, 2012). Hymenoptera represents a good candidate model system in which to investigate the dynamics of mitogenome rearrangement (Mao et al, 2014b); for example, 2 protein-coding genes (cox1 and nad2) and 10 tRNA genes are rearranged in Conostigmus (Mao and Dowton, 2014a), and a largescale translocation involving the control region was reported in the Taeniogonalos taihorina mitogenome (Wu et al, 2014).…”