Insights into the transcriptional and translational mechanisms of linear organellar chromosomes in the box jellyfish Alatina alata (Cnidaria: Medusozoa: Cubozoa)

Abstract

Background: In most animals, the mitochondrial genome is characterized by its small size, organization into a single circular molecule, and a relative conservation of the number of encoded genes. In box jellyfish (Cubozoa, Cnidaria), the mitochondrial genome is organized into 8 linear mito-chromosomes harboring between one and 4 genes each, including 2 extra protein-coding genes: mt-polB and orf314. Such an organization challenges the traditional view of mitochondrial DNA (mtDNA) expression in animals. In this study, we investigate the pattern of mitochondrial gene expression in the box jellyfish Alatina alata, as well as several key nuclear-encoded molecular pathways involved in the processing of mitochondrial gene transcription. Results: Read coverage of DNA-seq data is relatively uniform for all 8 mito-chromosomes, suggesting that each mito-chromosome is present in equimolar proportion in the mitochondrion. Comparison of DNA and RNA-seq based assemblies indicates that mito-chromosomes are transcribed into individual transcripts in which the beginning and ending are highly conserved. Expression levels for mt-polB and orf314 are similar to those of other mitochondrialencoded genes, which provides further evidence for them having functional roles in the mitochondrion. Survey of the transcriptome suggests recognition of the mitochondrial tRNA-Met by the cytoplasmic aminoacyl-tRNA synthetase counterpart and C-to-U editing of the cytoplasmic tRNA-Trp after import into the mitochondrion. Moreover, several mitochondrial ribosomal proteins appear to be lost. Conclusions: This study represents the first survey of mitochondrial gene expression of the linear multi-chromosomal mtDNA in box jellyfish (Cubozoa). Future exploration of small RNAs and the proteome of the mitochondrion will test the hypotheses presented herein.

The Highly Divergent Mitochondrial Genomes Indicate That the Booklouse,Liposcelis bostrychophila(Psocoptera: Liposcelididae) Is a Cryptic Species

“…However, there are two major exceptions: linear mt genomes and multipartite mt genomes. Linear mitochondrial chromosomes have been found in 26 species of cnidarians ( Warrior and Gall 1985 ; Kayal et al 2012 , 2016 ; Smith et al 2012 ; Zou et al 2012 ). Multipartite mt genomes have been found in nematodes ( Armstrong et al 2000 ; Phillips et al 2016 ), thrips ( Dickey et al 2015 ), booklice of the genus Liposcelis ( Wei et al 2012 ; Chen et al 2014 ), and parasitic lice ( Shao et al 2012 ; Jiang et al 2013 ; Dong et al 2014 ; Song et al 2014 ; Herd et al 2015 ).…”

Mitochondrial RNA processing in absence of tRNA punctuations in octocorals

“…However, such attempts are lacking for non-bilaterians. Information on the mitochondrial transcriptomes of sea anemone [46], hydrozoan [28] and jellyfish [29] have shown the potential complexity of mitochondrial transcription and highlighted the need for a better understanding of the evolutionary processes leading to different strategies of mitochondrial transcription and regulation.…”

“…This transcription model is, however, based on the study of a small number of bilaterians [19–22]. Recent studies on medusozoan members possessing linear mitogenomes do provide some insights into the mt-transcription in non-bilaterians [28, 29]. However, a detailed exploration of mitochondrial RNA processing and characterization of UTRs is still lacking for most non-bilaterian animals, including anthozoans with circular mitogenomes more similar to the stereotypical animal mitochondrial genomes.…”

Mitochondrial RNA processing in absence of tRNA punctuations in octocorals

“…However, such attempts are lacking for non-bilaterians. Information on the mitochondrial transcriptomes of sea anemone [53], hydrozoan [28] and jellyfish [29] have shown the potential complexity of mitochondrial transcription and highlighted the need for a better understanding of the evolutionary processes leading to different strategies of mitochondrial transcription and regulation. The processing of the mt-tRNAs interspersed in the mitogenomes of most animals provide a mechanism to liberate protein-coding mRNAs from polycistronic precursors, leading to their maturation and availability for translation [24].…”

“…This transcription model is, however, based on the study of a small number of bilaterians [19][20][21][22]. Recent studies on medusozoan members possessing linear mitogenomes do provide some insights into the mttranscription in non-bilaterians [28,29]. However, a detailed exploration of mitochondrial RNA processing and characterization of UTRs is still lacking for most non-bilaterian animals, including anthozoans with circular mitogenomes more similar to the stereotypical animal mitochondrial genomes.…”