Renfu Shao

Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle

As an obligatory parasite of humans, the body louse (Pediculus humanus humanus) is an important vector for human diseases, including epidemic typhus, relapsing fever, and trench fever. Here, we present genome sequences of the body louse and its primary bacterial endosymbiont Candidatus Riesia pediculicola. The body louse has the smallest known insect genome, spanning 108 Mb. Despite its status as an obligate parasite, it retains a remarkably complete basal insect repertoire of 10,773 protein-coding genes and 57 microRNAs. Representing hemimetabolous insects, the genome of the body louse thus provides a reference for studies of holometabolous insects. Compared with other insect genomes, the body louse genome contains significantly fewer genes associated with environmental sensing and response, including odorant and gustatory receptors and detoxifying enzymes. The unique architecture of the 18 minicircular mitochondrial chromosomes of the body louse may be linked to the loss of the gene encoding the mitochondrial single-stranded DNA binding protein. The genome of the obligatory louse endosymbiont Candidatus Riesia pediculicola encodes less than 600 genes on a short, linear chromosome and a circular plasmid. The plasmid harbors a unique arrangement of genes required for the synthesis of pantothenate, an essential vitamin deficient in the louse diet. The human body louse, its primary endosymbiont, and the bacterial pathogens that it vectors all possess genomes reduced in size compared with their free-living close relatives. Thus, the body louse genome project offers unique information and tools to use in advancing understanding of coevolution among vectors, symbionts, and pathogens.

The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus

The mitochondrial (mt) genomes of animals typically consist of a single circular chromosome that is approximately 16-kb long and has 37 genes. Our analyses of the sequence reads from the Human Body Louse Genome Project and the patterns of gel electrophoresis and Southern hybridization revealed a novel type of mt genome in the sucking louse, Pediculus humanus. Instead of having all mt genes on a single chromosome, the 37 mt genes of this louse are on 18 minicircular chromosomes. Each minicircular chromosome is 3-4 kb long and has one to three genes. Minicircular mt chromosomes are also present in the four other species of sucking lice that we investigated, but not in chewing lice nor in the Psocoptera, to which sucking lice are most closely related. We also report unequivocal evidence for recombination between minicircular mt chromosomes in P. humanus and for sequence variation in mt genes generated by recombination. The advantages of a fragmented mt genome, if any, are currently unknown. Fragmentation of mt genome, however, has coevolved with blood feeding in the sucking lice. It will be of interest to explore whether or not life history features are associated with the evolution of fragmented chromosomes.

Novel Mitochondrial Gene Content and Gene Arrangement Indicate Illegitimate Inter-mtDNA Recombination in the Chigger Mite, Leptotrombidium pallidum

To better understand the evolution of mitochondrial (mt) genomes in the Acari (mites and ticks), we sequenced the mt genome of the chigger mite, Leptotrombidium pallidum (Arthropoda: Acari: Acariformes). This genome is highly rearranged relative to that of the hypothetical ancestor of the arthropods and the other species of Acari studied. The mt genome of L. pallidum has two genes for large subunit rRNA, a pseudogene for small subunit rRNA, and four nearly identical large noncoding regions. Nineteen of the 22 tRNAs encoded by this genome apparently lack either a T-arm or a D-arm. Further, the mt genome of L. pallidum has two distantly separated sections with identical sequences but opposite orientations of transcription. This arrangement cannot be accounted for by homologous recombination or by previously known mechanisms of mt gene rearrangement. The most plausible explanation for the origin of this arrangement is illegitimate inter-mtDNA recombination, which has not been reported previously in animals. In light of the evidence from previous experiments on recombination in nuclear and mt genomes of animals, we propose a model of illegitimate inter-mtDNA recombination to account for the novel gene content and gene arrangement in the mt genome of L. pallidum.

Mitochondrial genomes of parasitic arthropods: implications for studies of population genetics and evolution.

Over 39000 species of arthropods parasitize humans, domestic animals and wildlife. Despite their medical, veterinary and economic importance, most aspects of the population genetics and evolution of the vast majority of parasitic arthropods are poorly understood. Mitochondrial genomes are a rich source of markers for studies of population genetics and evolution. These markers include (1) nucleotide sequences of each of the 37 mitochondrial genes and non-coding regions; (2) concatenated nucleotide sequences of 2 or more genes; and (3) genomic features, such as gene duplications, gene rearrangements, and changes in gene content and secondary structures of RNAs. To date, the mitochondrial genomes of over 700 species of multi-cellular animals have been sequenced entirely, however, only 24 of these species are parasitic arthropods. Of the mitochondrial genome markers, only the nucleotide sequences of 4 mitochondrial genes, cox1, cob, rrnS and rrnL, have been well explored in population genetic and evolutionary studies of parasitic arthropods whereas the sequences of the other 33 genes, and various genomic features have not. We review current knowledge of the mitochondrial genomes of parasitic arthropods, summarize applications of mitochondrial genes and genomic features in population genetic and evolutionary studies, and highlight prospects for future research.

Molecular Mechanisms for the Variation of Mitochondrial Gene Content and Gene Arrangement Among Chigger Mites of the Genus Leptotrombidium (Acari: Acariformes)

The gene content of a mitochondrial (mt) genome, i.e., 37 genes and a large noncoding region (LNR), is usually conserved in Metazoa. The arrangement of these genes and the LNR is generally conserved at low taxonomic levels but varies substantially at high levels. We report here a variation in mt gene content and gene arrangement among chigger mites of the genus Leptotrombidium. We found previously that the mt genome of Leptotrombidium pallidum has an extra gene for large-subunit rRNA (rrnL), a pseudo-gene for small-subunit rRNA (PrrnS), and three extra LNRs, additional to the 37 genes and an LNR typical of Metazoa. Further, the arrangement of mt genes of L. pallidum differs drastically from that of the hypothetical ancestor of the arthropods. To find to what extent the novel gene content and gene arrangement occurred in Leptotrombidium, we sequenced the entire or partial mt genomes of three other species, L. akamushi, L. deliense, and L. fletcheri. These three species share the arrangement of all genes with L. pallidum, except trnQ (for tRNA-glutamine). Unlike L. pallidum, however, these three species do not have extra rrnL or PrrnS and have only one extra LNR. By comparison between Leptotrombidium species and the ancestor of the arthropods, we propose that (1) the type of mt genome present in L. pallidum evolved from the type present in the other three Leptotrombidium species, and (2) three molecular mechanisms were involved in the evolution of mt gene content and gene arrangement in Leptotrombidium species.

Higher-level phylogeny of paraneopteran insects inferred from mitochondrial genome sequences

Mitochondrial (mt) genome data have been proven to be informative for animal phylogenetic studies but may also suffer from systematic errors, due to the effects of accelerated substitution rate and compositional heterogeneity. We analyzed the mt genomes of 25 insect species from the four paraneopteran orders, aiming to better understand how accelerated substitution rate and compositional heterogeneity affect the inferences of the higher-level phylogeny of this diverse group of hemimetabolous insects. We found substantial heterogeneity in base composition and contrasting rates in nucleotide substitution among these paraneopteran insects, which complicate the inference of higher-level phylogeny. The phylogenies inferred with concatenated sequences of mt genes using maximum likelihood and Bayesian methods and homogeneous models failed to recover Psocodea and Hemiptera as monophyletic groups but grouped, instead, the taxa that had accelerated substitution rates together, including Sternorrhyncha (a suborder of Hemiptera), Thysanoptera, Phthiraptera and Liposcelididae (a family of Psocoptera). Bayesian inference with nucleotide sequences and heterogeneous models (CAT and CAT + GTR), however, recovered Psocodea, Thysanoptera and Hemiptera each as a monophyletic group. Within Psocodea, Liposcelididae is more closely related to Phthiraptera than to other species of Psocoptera. Furthermore, Thysanoptera was recovered as the sister group to Hemiptera.

Extraordinary number of gene rearrangements in the mitochondrial genomes of lice (Phthiraptera: Insecta)

The arrangement of genes in the mitochondrial (mt) genomes of most insects is the same, or near‐identical, to that inferred to be ancestral for insects. We sequenced the entire mt genome of the small pigeon louse, Campanulotes bidentatus compar, and part of the mt genomes of nine other species of lice. These species were from six families and the three main suborders of the order Phthiraptera. There was no variation in gene arrangement among species within a family but there was much variation in gene arrangement among the three suborders of lice. There has been an extraordinary number of gene rearrangements in the mitochondrial genomes of lice!

The Multipartite Mitochondrial Genome of Liposcelis bostrychophila: Insights into the Evolution of Mitochondrial Genomes in Bilateral Animals

Booklice (order Psocoptera) in the genus Liposcelis are major pests to stored grains worldwide and are closely related to parasitic lice (order Phthiraptera). We sequenced the mitochondrial (mt) genome of Liposcelis bostrychophila and found that the typical single mt chromosome of bilateral animals has fragmented into and been replaced by two medium-sized chromosomes in this booklouse; each of these chromosomes has about half of the genes of the typical mt chromosome of bilateral animals. These mt chromosomes are 8,530 bp (mt chromosome I) and 7,933 bp (mt chromosome II) in size. Intriguingly, mt chromosome I is twice as abundant as chromosome II. It appears that the selection pressure for compact mt genomes in bilateral animals favors small mt chromosomes when small mt chromosomes co-exist with the typical large mt chromosomes. Thus, small mt chromosomes may have selective advantages over large mt chromosomes in bilateral animals. Phylogenetic analyses of mt genome sequences of Psocodea (i.e. Psocoptera plus Phthiraptera) indicate that: 1) the order Psocoptera (booklice and barklice) is paraphyletic; and 2) the order Phthiraptera (the parasitic lice) is monophyletic. Within parasitic lice, however, the suborder Ischnocera is paraphyletic; this differs from the traditional view that each suborder of parasitic lice is monophyletic.

The complete mitochondrial genomes of three parasitic nematodes of birds: a unique gene order and insights into nematode phylogeny.

BackgroundAnalyses of mitochondrial (mt) genome sequences in recent years challenge the current working hypothesis of Nematoda phylogeny proposed from morphology, ecology and nuclear small subunit rRNA gene sequences, and raise the need to sequence additional mt genomes for a broad range of nematode lineages.ResultsWe sequenced the complete mt genomes of three Ascaridia species (family Ascaridiidae) that infest chickens, pigeons and parrots, respectively. These three Ascaridia species have an identical arrangement of mt genes to each other but differ substantially from other nematodes. Phylogenetic analyses of the mt genome sequences of the Ascaridia species, together with 62 other nematode species, support the monophylies of seven high-level taxa of the phylum Nematoda: 1) the subclass Dorylaimia; 2) the orders Rhabditida, Trichinellida and Mermithida; 3) the suborder Rhabditina; and 4) the infraorders Spiruromorpha and Oxyuridomorpha. Analyses of mt genome sequences, however, reject the monophylies of the suborders Spirurina and Tylenchina, and the infraorders Rhabditomorpha, Panagrolaimomorpha and Tylenchomorpha. Monophyly of the infraorder Ascaridomorpha varies depending on the methods of phylogenetic analysis. The Ascaridomorpha was more closely related to the infraorders Rhabditomorpha and Diplogasteromorpha (suborder Rhabditina) than they were to the other two infraorders of the Spirurina: Oxyuridorpha and Spiruromorpha. The closer relationship among Ascaridomorpha, Rhabditomorpha and Diplogasteromorpha was also supported by a shared common pattern of mitochondrial gene arrangement.ConclusionsAnalyses of mitochondrial genome sequences and gene arrangement has provided novel insights into the phylogenetic relationships among several major lineages of nematodes. Many lineages of nematodes, however, are underrepresented or not represented in these analyses. Expanding taxon sampling is necessary for future phylogenetic studies of nematodes with mt genome sequences.

The mitochondrial genomes of soft ticks have an arrangement of genes that has remained unchanged for over 400 million years

There are two major groups of ticks: soft ticks and hard ticks. The hard ticks comprise the prostriate ticks and the metastriate ticks. The mitochondrial (mt) genomes of one species of prostriate tick and two species of metastriate ticks had been sequenced prior to our study. The prostriate tick has the ancestral arrangement of mt genes of arthropods, whereas the two metastriate ticks have rearrangements of eight genes and duplicate control regions. However, the arrangement of genes in the mt genomes of soft ticks had not been studied. We sequenced the mt genomes of two species of soft ticks, Carios capensis and Ornithodoros moubata, and a metastriate tick, Haemaphysalis flava. We found that the soft ticks have the ancestral arrangement of mt genes of arthropods, whereas the metastriate tick, H. flava, shares the rearrangements of mt genes and duplicate control regions with the other two metastriate ticks that have previously been studied. Our study indicates that gene rearrangements and duplicate control regions in mt genomes occurred once in the most recent common ancestor of metastriate ticks, whereas the ancestral arrangement of arthropods has remained unchanged for over 400 million years in the lineages leading to the soft ticks and the prostriate ticks.