Molluscan mitochondrial genomes break the rules

Abstract

The first animal mitochondrial genomes to be sequenced were of several vertebrates and model organisms, and the consistency of genomic features found has led to a 'textbook description'. However, a more broad phylogenetic sampling of complete animal mitochondrial genomes has found many cases where these features do not exist, and the phylum Mollusca is especially replete with these exceptions. The characterization of full mollusc mitogenomes required considerable effort involving challenging molecular biology, but has created an enormous catalogue of surprising deviations from that textbook description, including wide variation in size, radical genome rearrangements, gene duplications and losses, the introduction of novel genes, and a complex system of inheritance dubbed 'doubly uniparental inheritance'. Here, we review the extraordinary variation in architecture, molecular functioning and intergenerational transmission of molluscan mitochondrial genomes. Such features represent a great potential for the discovery of biological history, processes and functions that are novel for animal mitochondrial genomes. This provides a model system for studying the evolution and the manifold roles that mitochondria play in organismal physiology, and many ways that the study of mitochondrial genomes are useful for phylogeny and population biology. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.

Keywords: doubly uniparental inheritance; evolution; genome; mitochondria; mollusc.

Figure 1.

Relationship between the length of (a) non-coding and (b) coding regions on total mtDNA length in molluscan classes. Variation in non-coding length explains a greater proportion of variation in total mtDNA length compared to variation in coding length. Each circle represents a single species. When multiple mtDNAs were available for a single species, the mean across all individual records was taken as the species value. Colours represent different molluscan classes and are indicated by the key in (a).

Figure 2.

In mitogenomes of planobid gastropods, the atp8 gene is bracketed by trnN(aac) and trnL2(tta). Shaded boxes, tRNA genes; white boxes, protein-coding genes; arrowheads indicate directionality; asterisk, stop codon. ORF analyses of the mitogenome sequences that ignore the concept of tRNA gene excision from polycistronic mitogenomic transcripts frequently yield incorrect prediction of protein-coding sequence intervals. Whereas the start codon is correctly indicated, the ORF for atp8 from Biomphalaria glabrata (underlined in both nucleotide and predicted amino acid sequences, NC_005439) falls short, despite an effort to accommodate an incomplete stop codon (T--). Another issue impacts the ORF selected from the Planorbella duryi mitogenome (KY514384). It comprises a (correct) start codon and TAA stop codon but overlaps with trnL2 and yields an unusually long protein sequence. For both snail species, considering the boundaries of the (MITOS predicted) tRNA genes, the ATA is the first possible start codon downstream from trnN. At the 3′ end, a single T nucleotide remains after excision of trnL2, completed by polyadenylation to a TAA (underlined) stop codon. Such peculiarities challenge prediction of multiple genes from molluscan mitochondrial sequences, as is evidenced in several GenBank entries, despite the purported curation of submissions by this NCBI database. Re-evaluation and, if appropriate, updates by contributors of previous GenBank accessions will greatly benefit correct annotation.

Figure 3.

Top: Graphic showing the number of complete (dark colours) and partial (light colours: min. size 10 000 bp) mitogenomes available in GenBank; middle: mean, minimum and maximum size (bp) of complete mitogenomes per Mollusca class; bottom: graphic showing the percentage of total species with complete mitogenomes published in GenBank. Asterisk superscripts refer to unverified size values, due to assembly challenges; critical evaluation of these publicly available mitogenome sizes and sequence content is highly recommended.