Rapid evolution of the compact and unusual mitochondrial genome in the ctenophore, Pleurobrachia bachei

Abstract

Ctenophores are one of the most basally branching lineages of metazoans with the largest mitochondrial organelles in the animal kingdom. We sequenced the mitochondrial (mtDNA) genome from the Pacific cidipid ctenophore, Pleurobrachia bachei. The circular mitochondrial genome is 11,016 nts, with only 12 genes, and one of the smallest metazoan mtDNA genomes recorded. The protein coding genes are intronless cox1-3, cob, nad1, 3, 4, 4L and 5. The nad2 and 6 genes are represented as short fragments whereas the atp6 gene was found in the nuclear genome. Only the large ribosomal RNA subunit and 2 tRNAs were present with possibly the small subunit unidentifiable due to extensive fragmentation. The observed unique features of this mitochondrial genome suggest that nuclear and mitochondrial genomes have evolved at very different rates. This reduced mtDNA genome sharply contrasts with the very large sizes of mtDNA found in other basal metazoans including Porifera (sponges), and Placozoa (Trichoplax).

Genetic aspects of mitochondrial genome evolution

“…Like in cnidarians, ctenophoran mitogenomes have substantially reduced or even completely lost their mitochondrial encoded tRNA genes. The rRNAs as well as the protein coding sequences are highly derived in the Ctenophora, often leading to extremely long branches in phylogenetic analyses Kohn et al, 2011).…”

Population Genomics of Marine Zooplankton

“…The mitogenomes available for marine zooplankton species indicate a general trend of high intra-and interspecific variability. Rearrangement of gene order is exceptionally common and has been documented in amphipods (Ki et al 2010) and ctenophores (Kohn et al 2012), with some of the genes relocated to the nuclear genome (Pett et al 2011). …”

“…gov/Tigriopus_califo rnicus a genome size estimate independent of assembly (Jue et al 2016) b genome size estimate independent of assembly (Rasch et al 2004) c not available/not provided d genome size estimate independent of assembly (Wyngaard and Rasch 2000) Hwang et al (2014) 16,775 Ctenophora Mnemiopsis leidyi Pett et al (2011) 10,000 Pleurobrachia bachei Kohn et al (2012) 11,016 Chaetognatha Sagitta decipiens Miyamoto et al (2010) 11,121 Sagitta enflata Miyamoto et al (2010) 12,631 Sagitta ferox Li et al (2016) 12,153 Sagitta nagae Miyamoto et al (2010) 11,459 Paraspadella gotoi Helfenbein et al (2004) 11,423 Pterosagitta draco Wei et al (2016) 10,426 Spadella cephaloptera Papillon et al (2004) 11,905 Genome size (GB) …”

The ctenophore lineage is older than sponges? That cannot be right! Or can it?

“…There are no well-supported data that place the cnidarian lineage (anemones, corals and their relatives) or the bilaterian lineage (e.g. flatworms, mollusks, vertebrates, arthropods, annelids) at the base of the animal tree, but debate about lineages that lead to placozoans (small very simple amorphous animals), poriferans and ctenophores has been lively during the last 10 years (Dellaporta et al, 2006;Signorovitch et al, 2007;Dunn et al, 2008;Hejnol et al, 2009;Philippe et al, 2009;Schierwater et al, 2009;Srivastava et al, 2010;Kohn et al, 2012;Nosenko et al, 2013). More complete discussion of hypotheses concerning the evolution of early animals and data is presented in Halanych (Halanych, 2004), Kocot et al (Kocot et al, 2010) and Ryan et al (Ryan et al, 2013).…”

“…ATPase 9 and extra tRNAs), some sponges have a slightly larger mtDNA genome (approaching 20 kb) (Lavrov et al, 2005) and some cnidarians have linear mtDNA genomes (Bridge et al, 1992). Ctenophores, however, also have a highly divergent mtDNA genome ~11 kb in length and missing several genes -most tRNAs are absent (Pett et al, 2011;Kohn et al, 2012). Trees based on mtDNA amino acid datasets seem to be sensitive to taxonomic inclusion or phylogenetic methods.…”