Mitochondrial Genome Haplotype Hypervariation Within the Isopod Parasitic Nematode Thaumamermis cosgrovei

Abstract

Characterization of mitochondrial genomes from individual Thaumamermis cosgrovei nematodes, obligate parasites of the isopod Armadillidium vulgare, revealed that numerous mtDNA haplotypes, ranging in size from 19 to 34 kb, are maintained in several spatially separated isopod populations. The magnitude and frequency of conspecific mtDNA size variation is unprecedented among all studied size-polymorphic metazoan mitochondrial genomes. To understand the molecular basis of this hypervariation, complete nucleotide sequences of two T. cosgrovei mtDNA haplotypes were determined. A hypervariable segment, residing between the atp6 and rrnL genes, contributes exclusively to T. cosgrovei mtDNA size variation. Within this region, mtDNA coding genes and putative nonfunctional sequences have accumulated substitutions and are duplicated and rearranged to varying extents. Hypervariation at this level has enabled a first insight into the life history of T. cosgrovei. In five A. vulgare hosts infected with multiple nematodes, four carried nematodes with identical mtDNA haplotypes, suggesting that hosts may become infected by ingesting a recently hatched egg clutch or become parasitized by individuals from the same brood prior to dispersal of siblings within the soil.

The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida) — An idiosyncratic gene order and phylogenetic information for chromadorean nematodes

“…Trichinella spiralis where it is also encoded; Lavrov and Brown, 2001). All 36 genes are encoded on the same strand, as for all other chromadorean mtDNAs reported to date; this is relatively uncommon in other metazoan mtDNAs including those of enoplean nematodes (Boore, 1999;Hu and Gasser, 2006;Tang and Hyman, 2007). There are some overlaps between the genes, mainly 1-2 bp, but a long overlapping region (18 bp) is found between cox3 and trnP.…”

Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species

“…With respect to the other mt-encoded genes, the common content consists of 2 rRNA genes (rrnS and rrnL) and 13 protein-coding genes for subunits of the respiratory chain complexes (nad1-nad6; nad4L; cox1-cox3; cob; atp6; atp8). The two rRNA genes are always mitochondrially encoded, and their duplication is very rare, having been observed in only four species (rrnS is duplicated in the bivalve Crassostrea gigas and in distinct haplotypes of the pillbug nematode Thaumamermis cosgrovei (Milbury and Gaffney, 2005;Tang and Hyman, 2007); rrnL is duplicated in the chigger mite Leptotrombidium pallidum (Shao et al, 2005b); both rrnS and rrnL are duplicated in the large mt haplotype of the nematode Strelkovimermis spiculatus). Loss or acquisition of the protein-coding genes are also rather infrequent (Table 2), and the actual loss of genes remains sometimes ambiguous due to uncertainty in gene annotation or to the availability of incomplete mtDNA sequences (see the absence of nad3 and nad6 in the mite Metaseiulus occidentalis, Jeyaprakash and Hoy, 2007, and the absence of atp8 and nad6 in two Hexactinellida sponges, Haen et al, 2007, respectively).…”

“…An even more atypical AR variability has been found between distinct individuals of two enoplean obligate parasites, T. cosgrovei and S. spiculatus. In T. cosgrovei the mtDNAs of different individuals range in size from 19 to 34 kb, and greatly differ in the so-called hypervariable region of the genome (Tang and Hyman, 2007). In fact, the hypervariable segment is characterized by duplicated regions arranged in direct or inverted orientation, and contains both functional and non-functional genes organized in a shuffled gene order.…”

“…In fact, the hypervariable segment is characterized by duplicated regions arranged in direct or inverted orientation, and contains both functional and non-functional genes organized in a shuffled gene order. The remaining portion of the genome, defined as 'constant', has an identical gene order in all analysed T. cosgrovei individuals (Tang and Hyman, 2007). In S. spiculatus, the unpublished small and large mtDNA haplotypes differs at least for the duplication of both rRNA genes in the large haplotype.…”

“…The mtDNA of Nematoda is characterized by evolutionary dynamics strongly different from that of other metazoans, as it shows a fast nucleotide substitution rate , a very high AT content, and unusual characteristics related to the mitochondrial translational machinery, such as unique initiation codons (Wolstenholme, 1992;Hu et al, 2003b), unconventional cloverleaf tRNA structures with a TV-replacement loop (Okimoto and Wolstenholme, 1990) and small rRNAs whose reduced size is probably correlated with the unconventional tRNA structure (Okimoto et al, 1994). In addition, intra-genome recombination, a process likely absent in most metazoan mtDNAs, has been experimentally demonstrated in the enoplean Meloidogynes javanica (Lunt and Hyman, 1997), and is suggested to be the mechanism responsible of the intricate mtDNA AR found in the enoplean Romanomermis and Thaumamermis species (Azevedo and Hyman, 1993;Tang and Hyman, 2007). Recombination is also the more simple and plausible mechanism to explain mitochondrial gene inversions, which is the frequent exchange of coding strand observed in nematodes.…”