Inverted base composition skews and discontinuous mitochondrial genome architecture evolution in the Enoplea (Nematoda)

Abstract

Background: Within the class Enoplea, the earliest-branching lineages in the phylum Nematoda, the relatively highly conserved ancestral mitochondrial architecture of Trichinellida is in stark contrast to the rapidly evolving architecture of Dorylaimida and Mermithida. To better understand the evolution of mitogenomic architecture in this lineage, we sequenced the mitogenome of a fish parasite Pseudocapillaria tomentosa (Trichinellida: Capillariidae) and compared it to all available enoplean mitogenomes.

Results: P. tomentosa exhibited highly reduced noncoding regions (the largest was 98 bp), and a unique base composition among the Enoplea. We attributed the latter to the inverted GC skew (0.08) in comparison to the ancestral skew in Trichinellidae (-0.43 to -0.37). Capillariidae, Trichuridae and Longidoridae (Dorylaimida) generally exhibited low negative or low positive skews (-0.1 to 0.1), whereas Mermithidae exhibited fully inverted low skews (0 to 0.05). This is indicative of inversions in the strand replication order or otherwise disrupted replication mechanism in the lineages with reduced/inverted skews. Among the Trichinellida, Trichinellidae and Trichuridae have almost perfectly conserved architecture, whereas Capillariidae exhibit multiple rearrangements of tRNA genes. In contrast, Mermithidae (Mermithida) and Longidoridae (Dorylaimida) exhibit almost no similarity to the ancestral architecture.

Conclusions: Longidoridae exhibited more rearranged mitogenomic architecture than the hypervariable Mermithidae. Similar to the Chromadorea, the evolution of mitochondrial architecture in enoplean nematodes exhibits a strong discontinuity: lineages possessing a mostly conserved architecture over tens of millions of years are interspersed with lineages exhibiting architectural hypervariability. As Longidoridae also have some of the smallest metazoan mitochondrial genomes, they contradict the prediction that compact mitogenomes should be structurally stable. Lineages exhibiting inverted skews appear to represent the intermediate phase between the Trichinellidae (ancestral) and fully derived skews in Chromadorean mitogenomes (GC skews = 0.18 to 0.64). Multiple lines of evidence (CAT-GTR analysis in our study, a majority of previous mitogenomic results, and skew disruption scenarios) support the Dorylaimia split into two sister-clades: Dorylaimida + Mermithida and Trichinellida. However, skew inversions produce strong base composition biases, which can hamper phylogenetic and other evolutionary studies, so enoplean mitogenomes have to be used with utmost care in evolutionary studies.

Keywords: Capillariidae; Compositional heterogeneity; GC skew; Gene rearrangement; Inversion of the replication order; Mitogenome; Phylogeny; Pseudocapillaria tomentosa.

Fig. 1

Mitochondrial architecture and skews of enoplean mitogenomes. GC skews on the plus strand are shown as yellow bars, where negative values are to the left from the axis and positive to the right. The legend for the mitochondrial architecture is shown in the figure, with only NCRs larger than 200 bp shown. Species names are given with GenBank accession numbers. The family and order-level taxonomic identity is shown to the right. Pseudocapillaria tomentosa is highlighted in blue

Fig. 2

Mitochondrial phylogenomics of the Enoplea: Maximum Likelihood. The phylogram was inferred using the Maximum Likelihood methodology implemented in IQ-TREE and nucleotide sequences of 12 protein-coding genes. Bootstrap support values are shown on the braches (only the values < 100 are shown). Species names are given with GenBank accession numbers. The phylum, class, order, and family-level taxonomic identities are shown to the right

Fig. 3

Mitochondrial phylogenomics of the Enoplea: CAT-GTR. The phylogram was inferred using the CAT-GTR algorithm designed for compositional heterogeneity implemented in PhyloBayes and amino acid sequences of 12 protein-coding genes. Posterior probability values are shown on the braches (only the values < 1.0 are shown). Species names are given with GenBank accession numbers. The phylum, class, order, and family-level taxonomic identities are shown to the right