Structure and Evolution of the Atypical Mitochondrial Genome of Armadillidium vulgare (Isopoda, Crustacea)

Abstract

The crustacean isopod Armadillidium vulgare is characterized by an unusual approximately 42-kb-long mitochondrial genome consisting of two molecules co-occurring in mitochondria: a circular approximately 28-kb dimer formed by two approximately 14-kb monomers fused in opposite polarities and a linear approximately 14-kb monomer. Here we determined the nucleotide sequence of the fundamental monomeric unit of A. vulgare mitochondrial genome, to gain new insight into its structure and evolution. Our results suggest that the junction zone between monomers of the dimer structure is located in or near the control region. Direct sequencing indicated that the nucleotide sequences of the different monomer units are virtually identical. This suggests that gene conversion and/or replication processes play an important role in shaping nucleotide sequence variation in this mitochondrial genome. The only heteroplasmic site we identified predicts an alloacceptor tRNA change from tRNA(Ala) to tRNA(Val). Therefore, in A. vulgare, tRNA(Ala) and tRNA(Val) are found at the same locus in different monomers, ensuring that both tRNAs are present in mitochondria. The presence of this heteroplasmic site in all sequenced individuals suggests that the polymorphism is selectively maintained, probably because of the necessity of both tRNAs for maintaining proper mitochondrial functions. Thus, our results provide empirical evidence for the tRNA gene recruitment model of tRNA evolution. Moreover, interspecific comparisons showed that the A. vulgare mitochondrial gene order is highly derived compared to the putative ancestral arthropod type. By contrast, an overall high conservation of mitochondrial gene order is observed within crustacean isopods.

The first complete mitogenome of the South China deep‐sea giant isopod Bathynomus sp. (Crustacea: Isopoda: Cirolanidae) allows insights into the early mitogenomic evolution of isopods

“…The positions of trnE and trnW are changed to positions downstream of rrnS , which has not been found in other isopods to date. Finally, the nad1 gene is moved to a position downstream of nad3 and from the minus strand to the plus strand and this translocation is novel feature found only in isopods (Kilpert & Podsiadlowski, 2010; Kilpert et al., 2012; Marcade et al., 2007). …”

Large gene overlaps and tRNA processing in the compact mitochondrial genome of the crustaceanArmadillidium vulgare

“…Although it codes for the usual set of 13 protein-coding genes and two rRNA subunits, only a partial set of mitochondrial tRNA genes was identified by computational means. 20,25 This partial set of tRNA genes was however not sufficient to account for a size reduction of 1.8 kbp in comparison to average malacostraca mt genome. Additional size reduction is due to shortness of the control region, 24 but also to putative gene overlaps, implicating tRNA genes.…”

“…Multiple gene overlaps in the A. vulgare mt genome Complete sequencing of A. vulgare mt genome revealed potential large overlaps between genes, 20,25 with no functional demonstration. We further investigated the precise location of each expressed tRNA gene with regard to the other A. vulgare mt genes.…”

“…Finally, heteroplasmic mtDNA may allow for the presence of two tRNA genes with different anticodons at the same genome position, an example of "hidden" tRNA recently described in the mtDNA of Oniscidea. [20][21][22] Unfortunately, in most cases, experimental data to validate or invalidate the expression of tRNA candidates are mostly unavailable yet.…”

The complete mitochondrial genome of the subterranean crustaceanMetacrangonyx longipes(Amphipoda): A unique gene order and extremely short control region

“…Within the malacostracan peracarid order Amphipoda, only a partial mitogenome sequence is currently available in sequence databases: that of Parhyale hawaiiensis (Dana 1853), although it lacks of about 3 Kb including the rrnS gene and parts of rrnL and nad2, and also the control region (Cook et al 2005). In addition, in the peracarid order Isopoda one entire (Ligia oceanica) and two partial mitogenomes (Armadillidium vulgare and Idotea baltica) are known (Kilpert and Podsiadlowski 2006;Podsiadlowski and Bartolomaeus 2006;Marcadé et al 2007). The taxon sampling set for crustacean mitogenomes is quite poor because only 30 out of about 800 known crustacean families are represented (Martin and Davis 2001).…”