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      Fragmented mitochondrial genomes of the rat lice, Polyplax asiatica and Polyplax spinulosa: intra-genus variation in fragmentation pattern and a possible link between the extent of fragmentation and the length of life cycle

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          Abstract

          Background

          Blood-sucking lice (suborder Anoplura) parasitize eutherian mammals with 67% of the 540 described species found on rodents. The five species of blood-sucking lice that infest humans and pigs have fragmented mitochondrial genomes and differ substantially in the extent of fragmentation. To understand whether, or not, any life-history factors are linked to such variation, we sequenced the mt genomes of Polyplax asiatica and Polyplax spinulosa, collected from the greater bandicoot rat, Bandicota indica, and the Asian house rat, Rattus tanezumi, respectively.

          Results

          We identified all of the 37 mitochondrial genes common to animals in Polyplax asiatica and Polyplax spinulosa. The mitochondrial genes of these two rat lice are on 11 circular minichromosomes; each minichromosome is 2–4 kb long and has 2–7 genes. The two rat lice share the same pattern for the distribution of the protein-coding genes and ribosomal RNA genes over the minichromosomes, but differ in the pattern for the distribution of 8 of the 22 transfer RNA genes. The mitochondrial genomes of the Polyplax rat lice have 3.4 genes, on average, on each minichromosome and, thus, are less fragmented than those of the human lice (2.1 and 2.4 genes per minichromosome), but are more fragmented than those of the pig lice (4.1 genes per minichromosome).

          Conclusions

          Our results revealed distinct patterns of mitochondrial genome fragmentation within the genus Polyplax and, furthermore, indicated a possible inverse link between the extent of mitochondrial genome fragmentation and the length of life cycle of the blood-sucking lice.

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          Most cited references15

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          Identification of protein coding regions by database similarity search.

          Sequence similarity between a translated nucleotide sequence and a known biological protein can provide strong evidence for the presence of a homologous coding region, even between distantly related genes. The computer program BLASTX performed conceptual translation of a nucleotide query sequence followed by a protein database search in one programmatic step. We characterized the sensitivity of BLASTX recognition to the presence of substitution, insertion and deletion errors in the query sequence and to sequence divergence. Reading frames were reliably identified in the presence of 1% query errors, a rate that is typical for primary sequence data. BLASTX is appropriate for use in moderate and large scale sequencing projects at the earliest opportunity, when the data are most prone to containing errors.
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            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.
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              Key transitions in animal evolution: a mitochondrial DNA perspective.

              Animal mitochondrial DNA (mtDNA) is usually depicted as a small and very economically organized molecule with almost invariable gene content, stable gene order, a high rate of sequence evolution, and several unorthodox genetic features. Sampling across different animal phyla reveals that such a description applies primarily to mtDNA of bilaterian animals (such as arthropods or chordates). By contrast, mitochondrial genomes of nonbilaterian animals (phyla Cnidaria, Placozoa, and Porifera) display more variation in size and gene content and, in most cases, lack the genetic novelties associated with bilaterian mtDNA. Outside the Metazoa, mtDNA of the choanoflagellate Monosiga brevicollis, the closest unicellular out-group, is a much larger molecule that contains a large proportion of noncoding DNA, 1.5 times more genes, as well as several introns. Thus, changes in animal mtDNA organization appear to correlate with two main transitions in animal evolution: the origin of multicellularity and the origin of the Bilateria. Studies of mtDNA in nonbilaterian animals provide valuable insights into these transitions in the organization of mtDNA and also supply data for phylogenetic analyses of the relationships of early animals. Here I review recent progress in the understanding of nonbilaterian mtDNA and discuss the advantages and limitations of mitochondrial data sets for inferences about the phylogeny and evolution of animals.
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                Author and article information

                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central
                1471-2164
                2014
                18 January 2014
                : 15
                : 44
                Affiliations
                [1 ]Institute of Entomology, Guizhou University, and the Provincial Key Laboratory for Agricultural Pest Management in Mountainous Region, Guiyang 550025, China
                [2 ]Institute of Pathogens and Vectors, Dali University, and the Key Laboratory for Preventing and Controlling Plague in Yunnan Province, Dali 671000, China
                [3 ]GeneCology Research Centre, Faculty of Science, Health, Education and Engineering, University of the Sunshine Coast, Maroochydore, Queensland 4556, Australia
                Article
                1471-2164-15-44
                10.1186/1471-2164-15-44
                3901344
                24438034
                9ece3258-2af6-4ca1-8dea-ad210a538c7a
                Copyright © 2014 Dong et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 20 September 2013
                : 15 January 2014
                Categories
                Research Article

                Genetics
                sucking lice,chromosome evolution,minichromosome,genome fragmentation,mitochondrial genome

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