Background
A single circular mitochondrial (mt) genome is a common feature across most metazoans. The mt-genome includes protein-coding genes involved in oxidative phosphorylation, as well as RNAs necessary for translation of mt-RNAs, whose order and number are highly conserved across animal clades, with few known exceptions of alternative mt-gene order or mt-genome architectures. One such exception consists of the fragmented mitochondrial genome, a type of genome architecture where mt-genes are split across two or more mt-chromosomes. However, the origins of mt-genome fragmentation and its effects on mt-genome evolution are unknown. Here, we investigate these origin and potential mechanisms underlying mt-genome fragmentation, focusing on a genus of booklice, Liposcelis, which exhibits elevated sequence divergence, frequent rearrangement of mt-gene order, and fragmentation of the mt genome, and compare them to other Metazoan clades.
Results
We found this genus Liposcelis exhibits very low conservation of mt-gene order across species, relative to other metazoans. Levels of gene order rearrangement were, however, unrelated to whether or not mt-genomes were fragmented or intact, suggesting mitochondrial genome fragmentation is not affecting mt-gene order directly. We further investigated possible mechanisms underpinning these patterns and revealed very high conservation of non-coding sequences at the edges of multiple recombination regions across populations of one particular Liposcelis species, supportive of a hypothesis that mt-fragmentation arises from recombination errors between mt-genome copies. We propose these errors may arise as a consequence of a heightened mutation rate in clades exhibiting mt-fragmentation. Consistent with this, we observed a striking pattern across three Metazoan phyla (Arthropoda, Nematoda, Cnidaria) characterised by members exhibiting high levels of mt-gene order rearrangement and cases of mt-fragmentation, whereby the mt-genomes of species more closely related to species with fragmented mt-genomes diverge more rapidly despite experiencing strong purifying selection.
Conclusions
We showed that contrary to expectations, mt-genome fragmentation is not correlated with the increase in mt-genome rearrangements. Furthermore, we present evidence that fragmentation of the mt-genome may be part of a general relaxation of a natural selection on the mt-genome, thus providing new insights into the origins of mt-genome fragmentation and evolution.
The booklouse, Liposcelis bostrychophila is an important storage pest worldwide. The mitochondrial (mt) genome of an asexual strain (Beibei, China) of the L. bostrychophila comprises two chromosomes; each chromosome contains approximate half of the 37 genes typically found in bilateral animals. The mt genomes of two sexual strains of L. bostrychophila, however, comprise five and seven chromosomes, respectively; each chromosome contains one to six genes. To understand mt genome evolution in L. bostrychophila, and whether L. bostrychophila is a cryptic species, we sequenced the mt genomes of six strains of asexual L. bostrychophila collected from different locations in China, Croatia, and the United States. The mt genomes of all six asexual strains of L. bostrychophila have two chromosomes. Phylogenetic analysis of mt genome sequences divided nine strains of L. bostrychophila into four groups. Each group has a distinct mt genome organization and substantial sequence divergence (48.7–87.4%) from other groups. Furthermore, the seven asexual strains of L. bostrychophila, including the published Beibei strain, are more closely related to two other species of booklice, L. paeta and L. sculptilimacula, than to the sexual strains of L. bostrychophila. Our results revealed highly divergent mt genomes in the booklouse, L. bostrychophila, and indicate that L. bostrychophila is a cryptic species.
BackgroundBooklice (psocids) in the genus Liposcelis (Psocoptera: Liposcelididae) are a group of important storage pests, found in libraries, grain storages, and food-processing facilities. Booklice are able to survive under heat treatment and typically possess high resistance to common fumigant insecticides, hence posing a threat to storage security worldwide.ResultsWe assembled the genome of the booklouse, L. brunnea, the first genome reported in Psocoptera, using PacBio long-read sequencing, Illumina sequencing, and chromatin conformation capture (Hi-C) methods. After assembly, polishing, haplotype purging, and Hi-C scaffolding, we obtained 9 linkage groups (174.1 Mb in total) ranging from 12.1 Mb to 27.6 Mb (N50: 19.7 Mb), with the BUSCO completeness at 98.9%. In total, 15,543 genes were predicted by the Maker pipeline. Gene family analyses indicated the sensing-related gene families (OBP and OR) and the resistance-related gene families (ABC, EST, GST, UGT, and P450) expanded significantly in L. brunnea compared with those of their closest relatives (2 parasitic lice). Based on transcriptomic analysis, we found that the CYP4 subfamily from the P450 gene family functioned during phosphine fumigation; HSP genes, particularly those from the HSP70 subfamily, were upregulated significantly under high temperatures.ConclusionsWe present a chromosome-level genome assembly of L. brunnea, the first genome reported for the order Psocoptera. Our analyses provide new insights into the gene family evolution of the louse clade and the transcriptomic responses of booklice to environmental stresses.
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