The complete mitochondrial genome of Flustra foliacea (Ectoprocta, Cheilostomata) - compositional bias affects phylogenetic analyses of lophotrochozoan relationships

Abstract

BackgroundThe phylogenetic relationships of the lophophorate lineages, ectoprocts, brachiopods and phoronids, within Lophotrochozoa are still controversial. We sequenced an additional mitochondrial genome of the most species-rich lophophorate lineage, the ectoprocts. Although it is known that there are large differences in the nucleotide composition of mitochondrial sequences of different lineages as well as in the amino acid composition of the encoded proteins, this bias is often not considered in phylogenetic analyses. We applied several approaches for reducing compositional bias and saturation in the phylogenetic analyses of the mitochondrial sequences.ResultsThe complete mitochondrial genome (16,089 bp) of Flustra foliacea (Ectoprocta, Gymnolaemata, Cheilostomata) was sequenced. All protein-encoding, rRNA and tRNA genes are transcribed from the same strand. Flustra shares long intergenic sequences with the cheilostomate ectoproct Bugula, which might be a synapomorphy of these taxa. Further synapomorphies might be the loss of the DHU arm of the tRNA L(UUR), the loss of the DHU arm of the tRNA S(UCN) and the unique anticodon sequence GAG of the tRNA L(CUN). The gene order of the mitochondrial genome of Flustra differs strongly from that of the other known ectoprocts. Phylogenetic analyses of mitochondrial nucleotide and amino acid data sets show that the lophophorate lineages are more closely related to trochozoan phyla than to deuterostomes or ecdysozoans confirming the Lophotrochozoa hypothesis. Furthermore, they support the monophyly of Cheilostomata and Ectoprocta. However, the relationships of the lophophorate lineages within Lophotrochozoa differ strongly depending on the data set and the used method. Different approaches for reducing heterogeneity in nucleotide and amino acid data sets and saturation did not result in a more robust resolution of lophotrochozoan relationships.ConclusionThe contradictory and usually weakly supported phylogenetic reconstructions of the relationships among lophotrochozoan phyla based on mitochondrial sequences indicate that these alone do not contain enough information for a robust resolution of the relations of the lophotrochozoan phyla. The mitochondrial gene order is also not useful for inferring their phylogenetic relationships, because it is highly variable in ectoprocts, brachiopods and some other lophotrochozoan phyla. However, our study revealed several rare genomic changes like the evolution of long intergenic sequences and changes in the structure of tRNAs, which may be helpful for reconstructing ectoproct phylogeny.

Inheritance and phylogenetic analysis of Tylosurus acus melanotus based on the complete mitochondrial genomes

“…Similar to previous report, AT-Skew and GC-skews usually show high levels of variation, indicating the effects of phylogenetic analyses (Nesnidal et al 2011). The nucleotide skewness for the coding strands of T. acus melanotus (GC-skew ¼ À0.21, AT-skew ¼0.02) is biased towards A and C. A similar trend has been observed in other teleost mitogenomes: the negative GC-skew ranges from À0.53(ATP8) to À0.12(CO2) and the AT-skew showed more positive varying from À0.17(ND3) to 0.26(ATP6).…”

Comparative mitogenomic analyses reveal cryptic diversity of the bryozoan Bugula neritina Linnaeus, 1758, in the Yellow Sea

“…Samples were sequenced using the Illumina HiSeq 2000 platform (Illumina, San Diego, CA, USA), following the protocols supplied by Illumina. Reads were assembled using ABySS (kmer ¼ 30; Simpson et al 2009), and the contigs were then aligned with BLAST using the database of seven reported bryozoan mitochondrial genomes (Waeschenbach et al 2006;Jang and Hwang 2009;Sun et al 2009;Nesnidal et al 2011;Sun et al 2011;Shen et al 2012;Waeschenbach et al 2012). The largest matched contig is 15 101 bp in length.…”

“…With the mitochondrial genome sequence of B. neritina from China (QD), the currently available eight bryozoan mitochondrial genomes from GenBank were included in the phylogenetic analysis, including B. neritina from China (TG) (Jang and Hwang 2009), Celleporella hyalina (Waeschenbach et al 2012), Flustra foliacea (Nesnidal et al 2011), Flustrellidra hispida (Waeschenbach et al 2006), Membranipora grandicella (Shen et al 2012), Tubulipora flabellaris and Watersipora subtorquata ). In addition, 10 genera of Lophotrochozoa with at least two complete mitochondrial genomes reported, including Mytilus, Crassostrea, Hyriopsis, Meretrix, Sepiella, Aplysia, Potamopyrgu, Conus, Haliotis and Sypharochiton, were also incorporated in the analysis.…”

“…Every newly sequenced mitochondrial genome contains a novel gene arrangement, none of which is identical to those of the other bryozoans (Waeschenbach et al 2006;Jang and Hwang 2009;Sun et al 2009Sun et al , 2011Nesnidal et al 2011;Shen et al 2012;Waeschenbach et al 2012). In contrast, there is no variation in mitochondrial gene arrangements within each genus, including Aplysia (A. californica and A. dactylomela) (Knudsen et al 2006;Medina et al 2011), Crassostrea (C. angulata, C. gigas and C. sikamea) (Ren et al 2010), Haliotis (H. laevigata and H. rubra) (Maynard et al 2005;Robinson et al 2014), Hyriopsis (H. cumingii and H. schlegelii) (Wei et al 2014), Mytilus (M. edulis and M. galloprovincialis) Mizi et al 2005), Potamopyrgus (P. antipodarum and P. estuarinus) (Neiman et al 2010), Sepiella (S. inermis and S. japonica) (Wang et al 2013), Sypharochiton (S. pelliserpentis and S. sinclairi) (Veale Table 3…”

Mitochondrial Genomes of Kinorhyncha: trnM Duplication and New Gene Orders within Animals

“…It was suggested that changes in the mitochondrial gene order can be used as cladistic characters for studying relationships among higher-level taxa [ 3 ]. In some taxonomic groups such as insects and vertebrates the gene order tends to be conservative, while in some other groups such as Mollusca [ 4 ], Bryozoa [ 5 – 7 ], Acari [ 8 ], and Tunicata [ 9 , 10 ] it is highly variable. Generally, the taxon-specific gene order remains identical over long periods of time [ 11 – 13 ].…”