Rampant gene rearrangement and haplotype hypervariation among nematode mitochondrial genomes

Abstract

Rare syntenic conservation, sequence duplication, and the use of both DNA strands to encode genes are signature architectural features defining mitochondrial genomes of enoplean nematodes. These characteristics stand in contrast to the more conserved mitochondrial genome sizes and transcriptional organizations of mitochondrial DNAs (mtDNAs) derived from chromadorean nematodes. To address the frequency of gene rearrangement within nematode mitochondrial DNA (mtDNA), mitochondrial genome variation has been characterized within a more confined enoplean taxonomic unit, the family Mermithidae. The complete nucleotide sequences of the mosquito parasitic nematodes Romanomermis culicivorax, R. nielseni, and R. iyengari mtDNA have been determined. Duplicated expanses encompassing different regions of the mitochondrial genomes were found in each of these congeners. These mtDNA shared few rRNA and protein gene junctions, indicating extensive gene rearrangement within the Romanomermis lineage. Rapid structural changes are also observed at the conspecific level where no two individual nematodes carry the same haplotype. Rolling circle amplification was used to isolate complete mitochondrial genomes from individuals in local populations of Thaumamermis cosgrovei, a parasite of terrestrial isopods. Mitochondrial DNA length variants ranging from 19 to 34 kb are observed, but haplotypes are not shared between any two individuals. The complete nucleotide sequences of three haplotypes have been determined, revealing a constant region encoding most mitochondrial genes and a hypervariable segment that contains intact and pseudogene copies of several mitochondrial genes, duplicated to different copy numbers, resulting in mtDNA size variation. Constant rearrangement generates new T. cosgrovei mtDNA forms.

Intraspecific variability and genetic structure in Meloidogyne chitwoodi from the USA

“…Overall, we found a very high level of heteroplasmy in M. chitwoodi. Similar mtDNA haplotype hypervariation has been observed in other nematode species (Hyman et al, 2011) and might be a common phenomenon in the phylum as a whole.…”

Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes

“…This feature was also reported for the root-knot nematode Meloidogyne javanica (Tylenchoidea), which contains a 7 kb control region with different numbers of tandemly repeated sequence units [27]. In some Enoplea (mermithids), size variation ranging from 19 to 34 kb is relatively common and is attributed to a ‘hypervariable’ segment that includes both coding and putative nonfunctional regions (see [28] for more details). The complete mitochondrial genomes of B. xylophilus (Figure 1A) and P. vulnus (Figure 1B) contain 36 genes that comprise 12 protein-coding genes (PCGs) but lacking atp8 , 22 tRNA and 2 rRNA genes, all encoded in the same direction.…”

“…The mitochondrial NCR in many metazoans contains a sequence motif for replication origin (the control region) that varies from a few hundred bp to tens of kb, with tandemly repeated sequence blocks in a ‘head-to-tail’ fashion. The presence of lengthy repeated segments in non-coding regions is responsible for exceptionally large mtDNA genome size and often contributes to genome size variation among and within individuals (i.e., size-variant heteroplasmy) and/or species in some other metazoans including American shad [36], bark weevils [37], root-knot nematodes [27], scallops [38] and some mermithid nematodes [28,39]. Comparative analysis of size variants might be useful for estimating the genetic structure of populations within species and between closely related species [40].…”

Mitochondrial genome plasticity among species of the nematode genus Meloidogyne (Nematoda: Tylenchina)

“…In the phylum Nematoda mt genome plasticity among congeneric species has been reported mostly in the class Enoplea (Gissi et al, 2008). Different gene order in congeneric species has been observed in Romanomermis culicivorax, R. nielseni and R. iyengari, and different gene architecture among individuals of Thaumamermis cosgrovei, with sizes ranging from 19 to 34 kb (Hyman et al, 2011). In contrast, four congeneric species of Trichuris had identical gene arrangements (Liu et al, 2012a).…”