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The mitochondrial minichromosomes of the chimpanzee louse, Pediculus schaeffi. Each minichromosome has a coding region with gene names, transcription orientation, and length indicated, and a NCR in black. The minichromosomes are in alphabetical order according to the names of their protein-coding and rRNA genes, followed by those with tRNA genes only. Protein-coding genes are abbreviated as atp6 and atp8 (for ATP synthase subunits 6 and 8), cox1-3 (for cytochrome c oxidase subunits 1 to 3), cob (for cytochrome b), and nad1-6 and 4 L (for NADH dehydrogenase subunits 1 to 6 and 4 L). rrnL and rrnS are for large and small rRNA subunits. tRNA genes are shown with the single-letter abbreviations of their corresponding amino acids. Chimpanzee image: courtesy of the Tacugama Chimpanzee Sanctuary
Source publication
Blood-sucking lice in the genera Pediculus and Pthirus are obligate ectoparasites of great apes. Unlike most bilateral animals, which have 37 mitochondrial (mt) genes on a single circular chromosome, the sucking lice of humans have extensively fragmented mt genomes. The head louse, Pediculus capitis, and the body louse, Pe. humanus, have their 37 m...
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Sucking lice of the parvorder Anoplura are permanent ectoparasites with specific lifestyle and highly derived features. Currently, genomic data are only available for a single species, the human louse Pediculus humanus. Here, we present genomes of two distinct lineages, with different host spectra, of a rodent louse Polyplax serrata. Genomes of the...
Citations
... Incomplete codons TA (cox1 and cox2) and T (cox3, nad2 and nad3) were also used as stop codons, as in many other mt genomes e.g. Haematopinus (Jiang et al., 2013;Song et al., 2014), Polyplax Enderlein, 1904(Dong et al., 2014, Pediculus Linnaeus, 1758 (Herd et al., 2015), Microthoracius Fahrenholz, 1916(Shao et al., 2017, Hoplopleura Enderlein, 1904 (Fu et al., 2020a(Fu et al., , 2020b, and Pthirus Leach, 1815 species (Shao et al., 2012), and chewing lice, such as vulture lice Falcolipeurus quadripustulatus (Burmeister, 1838) (Song et al., 2019), elephant louse Haematomyzus elephantis Piaget, 1869 , and the screamer louse Bothriometopus macrocnemis (Burmeister, 1838) (Cameron et al., 2007). The rRNAs, rrnS and rrnL genes, were 721 bp and 1,161 bp in length, respectively. ...
The domestic pig louse Haematopinus suis (Linnaeus, 1758) (Phthiraptera: Anoplura) is a common ectoparasite of domestic pigs, which can act as a vector of various infectious disease agents. Despite its significance, the molecular genetics, biology and systematics of H. suis from China have not been studied in detail. In the present study, the entire mitochondrial (mt) genome of H. suis isolate from China was sequenced and compared with that of H. suis isolate from Australia. We identified 37 mt genes located on nine circular mt minichromosomes, 2.9 kb-4.2 kb in size, each containing 2-8 genes and one large non-coding region (NCR) (1,957 bp-2,226 bp). The number of minichromosomes, gene content, and gene order in H. suis isolates from China and Australia are identical. Total sequence identity across coding regions was 96.3% between H. suis isolates from China and Australia. For the 13 protein-coding genes, sequence differences ranged from 2.8%-6.5% consistent nucleotides with amino acids. Our result is H. suis isolates from China and Australia being the same H. suis species. The present study determined the entire mt genome of H. suis from China, providing additional genetic markers for studying the molecular genetics, biology and systematics of domestic pig louse.
... Among parasitic lice, chewing lice are in four parvorders: Amblycera, Ischnocera, Rhynchophthirina, and Trichodectera, while sucking lice are in the parvorder Anoplura [3]. Fragmented mitochondrial (mt) genomes have been found in 21 species of Anoplura [4][5][6][7][8][9][10][11][12][13][14], one species of Rhynchophthirina [15], and five species of Trichodectera [16,17]. Each of these species has 9 to 20 minichromosomes, which are usually less than 4 kb in size. ...
... The evidence available to date indicates that mt genome fragmentation occurred independently at least 14 times among parasitic lice (infraorder Phthiraptera): once in eutherian mammal lice in three parvorders (Anoplura, Rhynchophthirina, and Trichodectera) [16,20], four to five times in amblyceran lice ( [20], and the present study), and nine times in ischnoceran lice [20]. The independent evolution of fragmented mt genomes is also supported by the observations of the typical single-chromosome mt genomes in 16 amblyceran species from four different families (Boopiidae, Laemobothriidae, Menoponidae, and Ricinidae) ( [16,17,22,23], and the current study), in 10 ischnoceran species from 10 genera [16,18,21,41], but not in any species in Anoplura, Rhynchophthirina, or Trichodectera [4][5][6][7][8][9][10][11][12][13][14][15][16][17]. ...
... Song et al. [16] showed that mt genome fragmentation and minichromosomal characters united parasitic lice of eutherian mammals in three parvorders: Anoplura, Rhyn-chophthirina, and Trichodectera. All species in these three parvorders studied to date have fragmented mt genomes with a varying number of minichromosomes, from 9 to 20 in each species [4][5][6][7][8][9][10][11][12][13][14][15]17]. When only protein-coding and rRNA genes (these genes are more stable than tRNA genes in chromosomal locations) are considered, five minichromosomes, which contain cox1, nad4, nad5, rrnS, and rrnL, respectively, are in common among all eutherian mammal lice in these three parvorders, whereas other minichromosomes are variable [16]. ...
Mitochondrial (mt) genome fragmentation has been discovered in all five parvorders of parasitic lice (Phthiraptera). To explore whether minichromosomal characters derived from mt genome fragmentation are informative for phylogenetic studies, we sequenced the mt genomes of 17 species of bird lice in Menoponidae and Laemobothriidae (Amblycera). Four species of Menoponidae (Actornithophilus sp. 1 ex [pied oystercatcher], Act. sp. 2 ex [masked lapwing], Austromenopon sp. 2 ex [sooty tern and crested tern], Myr. sp. 1 ex [satin bowerbird]) have fragmented mt genomes, whereas the other 13 species retain the single-chromosome mt genomes. The two Actornithophilus species have five and six mt minichromosomes, respectively. Aus. sp. 2 ex [sooty tern and crested tern] has two mt minichromosomes, in contrast to Aus. sp. 1 ex [sooty shearwater], which has a single mt chromosome. Myr. sp. 1 ex [satin bowerbird] has four mt minichromosomes. When mapped on the phylogeny of Menoponidae and Laemobothriidae, it is evident that mt genome fragmentation has occurred multiple times independently among Menoponidae and Laemobothriidae species. We found derived mt minichromosomal characters shared between Myrsidea species, between Actornithophilus species, and between and among different ischnoceran genera, respectively. We conclude that while mt genome fragmentation as a general feature does not unite all the parasitic lice that have this feature, each independent mt genome fragmentation event does produce minichromosomal characters that can be informative for phylogenetic studies of parasitic lice at different taxonomic levels.
... and alignment Raw sequence-reads were de novo assembled to contigs level using Geneious (https://www.geneious.com) with the parameters: 1) minimum overlap identity, 95%; 2) minimum overlap, 50 bp; 3) maximum gaps per read, 10%; and 4) maximum gap size, 20 bp (Herd et al. 2015). DNA barcode region in the cox1 gene was used to distinguish the mt genome from all contigs. ...
... To date, reports on the mitochondrial genomes of aquatic animals have focused mainly on: (1) phylogenetic analyses, including relationship reconstructions; (2) between-species comparisons, such as through analysis of conserved gene clusters and determinations of the evolutionary conservation of species; (3) the phenomenon of gene rearrangements; (4) the mechanisms of tandem duplications; and (5) analyses of evolutionary selection pressures [14][15][16][17][18][19][20][21][22][23][24][25]. For instance, Tang et al. confirmed the status of the crab Helicana wuana (in the family Varunidae of subsection Thoracotremata) by analyzing the basic characteristics, gene arrangement, and phylogenetic inference of the mitochondrial genes [12]. ...
... Liu et al. compared structural characteristics of the mitochondrial genome and gene sequences among 16 bivalve species and found that the mitochondrial gene sequences were not obvious and their structures varied [26]. Iannelli et al. con- To date, reports on the mitochondrial genomes of aquatic animals have focused mainly on: (1) phylogenetic analyses, including relationship reconstructions; (2) between-species comparisons, such as through analysis of conserved gene clusters and determinations of the evolutionary conservation of species; (3) the phenomenon of gene rearrangements; (4) the mechanisms of tandem duplications; and (5) analyses of evolutionary selection pressures [14][15][16][17][18][19][20][21][22][23][24][25]. For instance, Tang et al. confirmed the status of the crab Helicana wuana (in the family Varunidae of subsection Thoracotremata) by analyzing the basic characteristics, gene arrangement, and phylogenetic inference of the mitochondrial genes [12]. ...
In natural sea areas along the coast of China, venerid clams Ruditapes philippinarum and R. variegatus exhibit similar adult shell forms and are especially difficult to distinguish as spat and juveniles. This study used comparative mitochondrial genome analysis to reveal differences between these species. The results showed that: (1) the mitochondrial genomes of R. philippinarum and R. variegatus share a large number of similar gene clusters arranged in consistent order, yet they also display noncommon genes, with both gene rearrangements and random losses found; (2) the 13 protein-coding genes in R. philippinarum as well as two-fold and four-fold degenerate sites in R. variegatus have an evident AT bias; (3) the Ka/Ks ratio of the mitochondrial ATP8 gene was significantly higher in R. philippinarum than in R. variegatus, and an analysis of selection pressure revealed that the mitochondrial NADH dehydrogenase subunit 2 gene and NADH dehydrogenase subunit 6 gene of R. variegatus were under great selective pressure during its evolution; and finally, (4) the two species clustered into one branch on a phylogenetic tree, further affirming their phylogenetic closeness. Based on these results, we speculate that the species differences between R. variegatus and R. philippinarum are largely attributable to adaptive evolution to the environment. The present findings provide a reference for the development of germplasm identification.
... An example of an extremely fragmented mt genome is the human body louse Pediculus humanus humanus with 20 mt minichromosomes [11]. To date, the mt genomes of 21 sucking lice species (12 complete mt genomes and 9 incomplete mt genomes) have been sequenced, all are extensively fragmented with different numbers of minichromosomes [11][12][13][14][15][16][17][18][19][20][21][22]. Often, mt gene arrangement and composition are stable among members of a louse genus [12,17,19]; however, substantial variation in mt 2 of 13 karyotype, the number of mt minichromosomes, gene arrangement and gene content has been also reported among congeneric lice, including sucking lice. ...
... To date, the mt genomes of 21 sucking lice species (12 complete mt genomes and 9 incomplete mt genomes) have been sequenced, all are extensively fragmented with different numbers of minichromosomes [11][12][13][14][15][16][17][18][19][20][21][22]. Often, mt gene arrangement and composition are stable among members of a louse genus [12,17,19]; however, substantial variation in mt 2 of 13 karyotype, the number of mt minichromosomes, gene arrangement and gene content has been also reported among congeneric lice, including sucking lice. In primate lice, the human louse P. humanus and chimpanzee louse P. schaeffi have 20 and 18 minichromosomes, respectively [12,17]. ...
... Often, mt gene arrangement and composition are stable among members of a louse genus [12,17,19]; however, substantial variation in mt 2 of 13 karyotype, the number of mt minichromosomes, gene arrangement and gene content has been also reported among congeneric lice, including sucking lice. In primate lice, the human louse P. humanus and chimpanzee louse P. schaeffi have 20 and 18 minichromosomes, respectively [12,17]. Macaque louse Pedicinus obtusus and colobus louse P. badii have 12 and 14 minichromosomes, respectively [19]. ...
Sucking lice are obligate ectoparasites of mammalian hosts, causing serious public health
problems and economic losses worldwide. It is well known that sucking lice have fragmented
mitochondrial (mt) genomes, but many remain undetermined. To better understand patterns of
mt genome fragmentation in the sucking lice, we sequenced the mt genome of the buffalo louse
Haematopinus tuberculatus using next-generation sequencing (NGS). The mt genome of H. tuberculatus
has ten circular minichromosomes containing a total of 37 genes. Each minichromosome is 2.9–5.0 kb
long and carries one to eight genes plus one large non-coding region. The number of mt minichromosomes
of H. tuberculatus (ten) is different from those of congeneric species (horse louse H. asini,
domestic pig louse H. suis and wild pig louse H. apri) and other sucking lice. Two events (gene
translocation and merger of mt minichromosome) are observed in Haematopinus. Compared to other
studies, our phylogeny generated from mt genome datasets showed a different topology, suggesting
that inclusion of data other than mt genomes would be required to resolve phylogeny of sucking lice.
To our knowledge, this is the first report of a ten mt minichromosomes genome in sucking lice, which
opens a new outlook into unexplored mt genome fragmentation patterns in sucking lice.
... Fragmented mitogenomes in lice were first described in the human body louse (Pediculus humanus corporis), which have 20 circular fragments ("minicircles") each containing 1-3 genes 12 . Subsequent studies indicated that fragmented mitogenomes in lice were ancestral in a clade of "mammal" lice (Parvorders Anoplura, Rhynchophthirina, and Trichodectera) [14][15][16][17][18][19] including the human louse, but more recent studies suggest mitogenome fragmentation is more widespread, although perhaps sporadic, across lice 13 . In agreement with these findings, full or partial mitogenomes with multiple chromosomes have been reported from a genus in Ischnocera (Columbicola) 20 and from several genera in Amblycera 21 , indicating that mitogenome fragmentation evolved multiple times within lice. ...
... However, it is unknown how stable the mitogenome organization is among individuals (or populations) within a species of louse. Heteroplasmy can also be present in some mitogenomes of lice, either in the form of divergence between homologous genes or multiple chromosomal arrangements within a single individual 13,18,22 . These reported cases suggest heteroplasmy could be much more prevalent in parasitic lice, particularly in lice with fragmented mitogenomes. ...
The mitochondrial genomes (mitogenomes) of bilaterian animals are highly conserved structures that usually consist of a single circular chromosome. However, several species of parasitic lice (Insecta: Phthiraptera) possess fragmented mitogenomes, where the mitochondrial genes are present on separate, circular chromosomes. Nevertheless, the extent, causes, and consequences of this structural variation remain poorly understood. Here, we combined new and existing data to better understand the evolution of mitogenome fragmentation in major groups of parasitic lice. We found strong evidence that fragmented mitogenomes evolved many times within parasitic lice and that the level of fragmentation is highly variable, including examples of heteroplasmic arrangements. We also found a significant association between mitochondrial fragmentation and signatures of relaxed selection. Mitochondrial fragmentation was also associated with changes to a lower AT%, possibly due to differences in mutation biases. Together, our results provide a significant advance in understanding the process of mitogenome fragmentation and provide an important perspective on mitochondrial evolution in eukaryotes. Multiple independent origins of fragmented mitochondrial genome evolution in parasitic lice provide insights into eukaryotic mitochondrial evolution.
... Fifteen species of sucking lice from seven of the 15 families have been sequenced for complete or near complete mt genomes [5][6][7][8][9][10][11][12][13]. Human head louse (Pediculus humanus capitis, family Pediculidae) and human body louse (Pediculus humanus corporis) have the most fragmented mt genomes with 20 minichromosomes [5,6], followed by chimpanzee louse (Pediculus schaeffi) with 18 minichromosomes [14]. Human pubic louse (Pthirus pubis, family Pthiridae) has 15 minichromosomes (trnN gene not identified) [6,12]. ...
Background
The mitochondrial (mt) genomes of 15 species of sucking lice from seven families have been studied to date. These louse species have highly dynamic, fragmented mt genomes that differ in the number of minichromosomes, the gene content, and gene order in a minichromosome between families and even between species of the same genus.
Results
In the present study, we analyzed the publicly available data to understand mt genome fragmentation in seal lice (family Echinophthiriidae) and gorilla louse, Pthirus gorillae (family Pthiridae), in particular the role of minichromosome split and minichromosome merger in the evolution of fragmented mt genomes. We show that 1) at least three ancestral mt minichromosomes of sucking lice have split in the lineage leading to seal lice, 2) one minichromosome ancestral to primate lice has split in the lineage to the gorilla louse, and 3) two ancestral minichromosomes of seal lice have merged in the lineage to the northern fur seal louse. Minichromosome split occurred 15-16 times in total in the lineages leading to species in six families of sucking lice investigated. In contrast, minichromosome merger occurred only four times in the lineages leading to species in three families of sucking lice. Further, three ancestral mt minichromosomes of sucking lice have split multiple times independently in different lineages of sucking lice. Our analyses of mt karyotypes and gene sequences also indicate the possibility of a host switch of crabeater seal louse to Weddell seals.
Conclusions
We conclude that: 1) minichromosome split contributes more than minichromosome merger in mt genome fragmentation of sucking lice, and 2) mt karyotype comparison helps understand the phylogenetic relationships between sucking louse species.
... Metazoan mitochondrial (mt) genomes are usually circular DNA organization (13-20 kb) that contain 36 to 37 genes: 12-13 proteincoding genes, two ribosomal RNA genes, and 22 transfer RNA genes (Boore, 1999;Lavrov, 2007;Wolstenholme, 1992). However, fragmented mt genomes have been reported from all sequenced blood-sucking lice (Dong et al., 2014a, b;Herd et al., 2015;Fu et al., 2020a, b;Jiang et al., 2013;Shao et al., 2012Shao et al., , 2015Shao et al., , 2017Song et al., 2014) and some chewing lice (Song et al., 2019;Sweet et al., 2020Sweet et al., , 2021. Although the suborder Anoplura contains 540 species of blood-sucking lice (Durden and Musser, 1994;Kim and Ludwig, 1978), to date, only mt genomes of 15 blood-sucking louse species have been sequenced and deposited in GenBank. ...
... The use of the start codon and stop codon of these protein-coding genes in wild pig louse H. apri from China is consistent with that in wild pig louse H. apri from Japan, except for nad4 gene (use ATG for Japan). Incomplete termination codons (TA and T) are also present in other sucking lice, including horse louse H. asini (Song et al., 2014), rat louse Hoplopleura kitti (Dong et al., 2014b), rat louse Polyplax asiatica (Dong et al., 2014a) and P. spinulosa (Dong et al., 2014a), chimpanzee louse Pediculus schaeffi (Herd et al., 2015), guanaco louse Microthoracius praelongiceps (Shao et al., 2017) and pubic louse Pthirus pubis (Shao et al., 2012). In the mt genome of wild pig louse H. apri from China, the sizes of the rrnL and rrnS genes were 718 bp and 1160 bp, respectively. ...
The wild pig louse Haematopinus apri is one of the commonest ectoparasites of wild pigs. In the present study, the entire mitochondrial (mt) genome of wild pig louse H. apri from China was sequenced and compared with previously characterized wild pig louse H. apri from Japan. We identified all of the 37 mt genes in the wild pig louse H. apri from China which are on nine circular minichromosomes. Each mt minichromosome is 2.9 kb–4.2 kb size and contains 2–8 genes and one non-coding region (1543 bp-2534 bp). The number of minichromosomes, gene content and gene order in the both mt genomes of wild pig louse H. apri from China and Japan is the same. The identity of the both mt genomes (except for non-coding regions) was 98.3% between wild pig louse H. apri from China and Japan. The entire mt genome sequence (except for non-coding regions) of wild pig louse H. apri from China is longer (3 bp) than that from Japan. For the 13 protein-coding genes, this comparison showed sequence differences in each gene at both the nucleotide (0.8%–2.4%) and amino acid (0.4%–3.5%) levels. The most conserved of these genes was the nad6, whereas the nad2 was least conserved at the nucleotide levels. This is the first comprehensive comparison of the mt genomes of a louse species from different geographic locations. This useful data provides additional genetic markers to study the phylogeny, systematics and population genetics of wild pig louse H. apri.
... Extensive fragmentation of mitochondrial (mt) genome was discovered first in three species of human lice, in which the single mt chromosome typical of animals evolved into 14 and 20 minichromosomes; each minichromosome has 1-5 genes and is 1.8-4 kb in size [1,2]. Since then, 26 more species of parasitic lice have been sequenced for mt genomes [3][4][5][6][7][8][9][10][11][12]. It appears that mt genome fragmentation occurred at least twice in parasitic lice: once 60-90 million years ago (MYA) in the most recent common ancestor of Mitodivisia -a newly identified clade that contains the vast majority of parasitic lice of eutherian mammals [10,[13][14][15], and later~25 MYA in the feather lice of the genus Columbicola [11,13]. ...
... Note: translocated tRNA genes in the MRCA of Polyplax lice are in bold T-nad1-Q-N-C Pedicinus badii [12] Yes No T-nad1-Q-N-G-nad3-W Pedicinus obtusus [12] Yes No E E-cob-S 1 -S 2 cob-S 1 -N-E-M Pediculus schaeffi [7] Yes No F-nad6-E-M Pthirus pubis [2] Yes No ...
... Haematopinus suis [3] Haematopinus asini [6] G-nad3-V-W-S 2 Pthirus pubis [2] Yes Yes I I-cox1-L 2 P-nad2-I Pediculus schaeffi [7] Yes Yes ...
Background
The typical single-chromosome mitochondrial (mt) genome of animals has fragmented into multiple minichromosomes in the lineage Mitodivisia, which contains most of the parasitic lice of eutherian mammals. These parasitic lice differ from each other even among congeneric species in mt karyotype, i.e. the number of minichromosomes, and the gene content and gene order in each minichromosome, which is in stark contrast to the extremely conserved single-chromosome mt genomes across most animal lineages. How fragmented mt genomes evolved is still poorly understood. We use Polyplax sucking lice as a model to investigate how tRNA gene translocation shapes the dynamic mt karyotypes.
Results
We sequenced the full mt genome of the Asian grey shrew louse, Polyplax reclinata . We then inferred the ancestral mt karyotype for Polyplax lice and compared it with the mt karyotypes of the three Polyplax species sequenced to date. We found that tRNA genes were entirely responsible for mt karyotype variation among these three species of Polyplax lice. Furthermore, tRNA gene translocation observed in Polyplax lice was only between different types of minichromosomes and towards the boundaries with the control region. A similar pattern of tRNA gene translocation can also been seen in other sucking lice with fragmented mt genomes.
Conclusions
We conclude that inter-minichromosomal tRNA gene translocation orientated towards the boundaries with the control region is a major contributing factor to the highly dynamic mitochondrial genome organization in the parasitic lice of mammals.
... Postmortem examination of small ruminants revealed a high infection rate in goats in China [2]. More than 15 Ostertagia species have been reported in small ruminants [3][4][5]. Among them, Ostertagia trifurcata (O. ...
... The mt genome is maternally inherited, and has stable genes, a variable gene arrangement and a faster gene evolution rate [10][11][12]. These features make them widely applicable in epidemiological studies, population genetics and phylogenetic relationships at different taxonomic levels [13][14][15][16][17]. ...
The complete mitochondrial (mt) genome of Ostertagia trifurcata, a parasitic nematode of small ruminants, has been sequenced and its phylogenetic relationship with selected members from the superfamily Trichostrongyloidea was investigated on the basis of deduced datasets of mt amino acid sequences. The entire mt genome of Ostertagia trifurcata is circular and 14,151 bp in length. It consists of a total of 36 genes comprising 12 genes coding for proteins (PCGs), 2 genes for ribosomal RNA (rRNA), 22 transfer RNA (tRNA) genes and 2 non-coding regions, since all genes are transcribed in the same direction. The phylogenetic analysis based on the concatenated datasets of predicted amino acid sequences of the 12 protein coding genes supported monophylies of the Haemonchidae, Dictyocaulidae and Molineidae families, but rejected monophylies of the Trichostrongylidae family. The complete characterization and provision of the mtDNA sequence of Ostertagia trifurcata provides novel genetic markers for molecular epidemiological investigations, systematics, diagnostics and population genetics of Ostertagia trifurcata and its correspondents.
