A comparative study of nemertean complete mitochondrial genomes, including two new ones for Nectonemertes cf. mirabilis and Zygeupolia rubens, may elucidate the fundamental pattern for the phylum Nemertea

Abstract

BackgroundThe mitochondrial genome is important for studying genome evolution as well as reconstructing the phylogeny of organisms. Complete mitochondrial genome sequences have been reported for more than 2200 metazoans, mainly vertebrates and arthropods. To date, from a total of about 1275 described nemertean species, only three complete and two partial mitochondrial DNA sequences from nemerteans have been published. Here, we report the entire mitochondrial genomes for two more nemertean species: Nectonemertes cf. mirabilis and Zygeupolia rubens.ResultsThe sizes of the entire mitochondrial genomes are 15365 bp for N. cf. mirabilis and 15513 bp for Z. rubens. Each circular genome contains 37 genes and an AT-rich non-coding region, and overall nucleotide composition is AT-rich. In both species, there is significant strand asymmetry in the distribution of nucleotides, with the coding strand being richer in T than A and in G than C. The AT-rich non-coding regions of the two genomes have some repeat sequences and stem-loop structures, both of which may be associated with the initiation of replication or transcription. The 22 tRNAs show variable substitution patterns in nemerteans, with higher sequence conservation in genes located on the H strand. Gene arrangement of N. cf. mirabilis is identical to that of Paranemertes cf. peregrina, both of which are Hoplonemertea, while that of Z. rubens is the same as in Lineus viridis, both of which are Heteronemertea. Comparison of the gene arrangements and phylogenomic analysis based on concatenated nucleotide sequences of the 12 mitochondrial protein-coding genes revealed that species with closer relationships share more identical gene blocks.ConclusionThe two new mitochondrial genomes share many features, including gene contents, with other known nemertean mitochondrial genomes. The tRNA families display a composite substitution pathway. Gene order comparison to the proposed ground pattern of Bilateria and some lophotrochozoans suggests that the nemertean ancestral mitochondrial gene order most closely resembles the heteronemertean type. Phylogenetic analysis proposes a sister-group relationship between Hetero- and Hoplonemertea, which supports one of two recent alternative hypotheses of nemertean phylogeny.

Sequencing of the complete mitochondrial genome of a fish-parasitic flatworm Paratetraonchoides inermis (Platyhelminthes: Monogenea): tRNA gene arrangement reshuffling and implications for phylogeny

“…Except for Tetrancistrum nebulosi (Young, 1967), the most abundant codon families were Leu2, Ile, and Phe. This is comparable to Lepidoptera [ 43 ] and Nemertea [ 44 ]. Noteworthy, the studied mt genome exhibited a strong preference for the A + T-rich members of these four codon families (>10%, Phe, Ile, Leu2 and Asn in Fig.…”

Evolution of mitochondrial gene order in Annelida

“…In contrast, all represented taxa branching from the base of the annelid tree show a completely different arrangement of genes than observed in Pleistoannelida, but the reconstruction of a putative annelid mitochondrial ground pattern still remains difficult. However, as already mentioned, it seems very likely that all genes were encoded on one strand except for tRNA-P and tRNA-T, as found in the two annelids Owenia fusiformis and Magelona mirabilis and in the ground pattern of Nemertea(Chen et al, 2012;Chen et al, 2011). Additionally,…”

“…The mitochondrial genes in brachiopods are generally encoded on one strand(Helfenbein et al, 2001) and in molluscs there is no general pattern. Different families of molluscs show a high diversity in strand usage and gene order(Osca et al, 2014).Interestingly, all but one mitochondrial genome of Nemertea, which are either sister group to Annelida or very closely related to them(Dunn et al, 2008; Laumer et al, 2015;Weigert et al, 2014), show a similar pattern to that found in Owenia fusiformis and Magelona mirabilis, where all genes are transcribed from one strand except for the two tRNAs encoding for threonine and proline (e.g (Chen et al, 2012;Chen et al, 2011)…”

“…In some species of Mollusca, Brachiopoda, Nemertea and Phoronida this gene boundary is disrupted (Boore, 2006;Chen et al, 2012;Helfenbein and Boore, 2004;Helfenbein et al, 2001;Noguchi et al, 2000). In Platyhelminthes, Acoelomorpha and Acanthocephala, the ATP8 gene is missing (Mwinyi et al, 2010;Steinauer et al, 2005;Valles and Boore, 2006).…”

A shore-based preliminary survey of marine ribbon worms (Nemertea) from the Caribbean coast of Colombia

“…Nevertheless, several species are known to have important effects as active predators, especially on mollusks, crustaceans and annelids ( Roe 1976 ; Thiel and Kruse 2001 ; Caplins and Turbeville 2011 ). Nemerteans also have caught the attention of different biological fields such as regeneration ( Coe 1934 , 1943 ), developmental biology ( Martindale and Henry 1995 ; Maslakova et al 2004 ), genetics ( Andrade et al 2012 ; Chen et al 2012 ), and pharmacology ( Kem et al 2006 ).…”