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’.

Mitochondrial Genomic Landscape: A Portrait of the Mitochondrial Genome 40 Years after the First Complete Sequence

“…Nonetheless, several exceptions have been observed. For instance, the atp8 gene is often very divergent (e.g., [89,105,106]) and in some cases it has been claimed to be completely absent ( [78,[107][108][109][110][111][112][113]; also see [88,114,115]). Furthermore, many Open Reading Frames (ORFs) with no clear homology have been detected in many bilaterian lineages (e.g., [89,103,[116][117][118][119][120][121]).…”

“…A handful of tRNAs have been identified in cnidarians (e.g., [78,123]), where additional genes are present ( [124] and references therein); similarly, many genes that are usually found in animal mtDNA are missing from that of ctenophores (tRNAs, atp6, atp8; [79,81,116,125]). This summary of mitochondrial molecular structures and architectures certainly gives an idea of the stunning variability of these organellar genomes, which largely surpasses that of plastid trans-splicing phenomena [19,78,81,126]; the use of different genetic codes [13,127,128]; bewildering gene rearrangement [81][82][83][84][85][86][87][88]105,106,[129][130][131]; and biparental and doubly uniparental inheritance [28,30,58,[132][133][134][135][136].…”

“…Moreover, phenomena of the punctuated expansion of mtDNA have been reported within clades with generally reduced genome size (e.g., frogs [ 85 ], ark shells [ 86 , 87 ]). In most cases, this variability is not related to gene content; rather, the expansion and reduction of the intergenic region appear to be the main drivers of genome size among eukaryotes (e.g., [ 38 , 56 , 58 , 82 , 83 , 88 , 89 ]).…”

“…This summary of mitochondrial molecular structures and architectures certainly gives an idea of the stunning variability of these organellar genomes, which largely surpasses that of plastid trans-splicing phenomena [ 19 , 78 , 81 , 126 ]; the use of different genetic codes [ 13 , 127 , 128 ]; bewildering gene rearrangement [ 81 , 82 , 83 , 84 , 85 , 86 , 87 , 88 , 105 , 106 , 129 , 130 , 131 ]; and biparental and doubly uniparental inheritance [ 28 , 30 , 58 , 132 , 133 , 134 , 135 , 136 ].…”

Pearls of wisdom—a Theo Murphy issue on molluscan genomics

“…Ghiselli et al . [19] highlight the remarkable nature of the mitochondrial genomes of some molluscs, which provide a model system for studying mitochondrial evolution. The mitochondrial genomes of molluscs highlight the manifold roles that mitochondria play in organismal physiology and the many ways that the study of mitochondrial genomes is useful for phylogeny and population biology.…”