Comparing the mitochondrial genomes of Wolbachia-dependent and independent filarial nematode species

Abstract

BackgroundMany species of filarial nematodes depend on Wolbachia endobacteria to carry out their life cycle. Other species are naturally Wolbachia-free. The biological mechanisms underpinning Wolbachia-dependence and independence in filarial nematodes are not known. Previous studies have indicated that Wolbachia have an impact on mitochondrial gene expression, which may suggest a role in energy metabolism. If Wolbachia can supplement host energy metabolism, reduced mitochondrial function in infected filarial species may account for Wolbachia-dependence. Wolbachia also have a strong influence on mitochondrial evolution due to vertical co-transmission. This could drive alterations in mitochondrial genome sequence in infected species. Comparisons between the mitochondrial genome sequences of Wolbachia-dependent and independent filarial worms may reveal differences indicative of altered mitochondrial function.ResultsThe mitochondrial genomes of 5 species of filarial nematodes, Acanthocheilonema viteae, Chandlerella quiscali, Loa loa, Onchocerca flexuosa, and Wuchereria bancrofti, were sequenced, annotated and compared with available mitochondrial genome sequences from Brugia malayi, Dirofilaria immitis, Onchocerca volvulus and Setaria digitata. B. malayi, D. immitis, O. volvulus and W. bancrofti are Wolbachia-dependent while A. viteae, C. quiscali, L. loa, O. flexuosa and S. digitata are Wolbachia-free. The 9 mitochondrial genomes were similar in size and AT content and encoded the same 12 protein-coding genes, 22 tRNAs and 2 rRNAs. Synteny was perfectly preserved in all species except C. quiscali, which had a different order for 5 tRNA genes. Protein-coding genes were expressed at the RNA level in all examined species. In phylogenetic trees based on mitochondrial protein-coding sequences, species did not cluster according to Wolbachia dependence.ConclusionsThus far, no discernable differences were detected between the mitochondrial genome sequences of Wolbachia-dependent and independent species. Additional research will be needed to determine whether mitochondria from Wolbachia-dependent filarial species show reduced function in comparison to the mitochondria of Wolbachia-independent species despite their sequence-level similarities.

Mitochondrial genome plasticity among species of the nematode genus Meloidogyne (Nematoda: Tylenchina)

“…It is thought that genome architecture in Chromadorea is more stable, having only a few differences in the NCRs (Gissi et al, 2008), e.g., two congeneric species of Caenorhabditis differ only in the number and size of NCRs. Similarly, identical gene arrangement among congeneric species has been reported in two species each of Ancylostoma (Hu et al, 2002;Jex et al, 2009), Metastrongylus (Jex et al, 2010), Trichostrongylus (Jex et al, 2010), Oesophagostomum (Lin et al, 2012), Ascaris (Liu et al, 2012b), Onchocerca (Keddie et al, 1998;McNulty et al, 2012), Bursaphelenchus (Sultana et al, 2013a), Bunostomum (Gao et al, 2014), three species each of Angiostrongylus (Lv et al, 2012;Gasser et al, 2012), Toxocara (Li et al, 2008), Ascaridia (Liu et al, 2013) and four species of Baylisascaris (Xie et al, 2011a,b).…”

“…Three initiation codons (ATT, TTA and ATA) are used in the mt genomes of M. arenaria, M. enterolobii and M. javanica. The start codon TTA is not commonly found in other nematodes, and has so far only been detected in the PPNs M. chitwoodi (nad6, nad4L, cob and nad5), M. incognita (cox1, nad6, cox2, nad3 and nad5) and R. similis (cox2 and nad5) (Jacob et al, 2009; and in the animal and human-parasitic nematodes Steinernema carpocapsae (nad2, nad4 and nad6), Brugia malayi (nad2), Wuchereria bancrofti (nad2), Onchocerca flexuosa (nad4L and nad5) and Ancylostoma doudenale (cox1) (Hu et al, 2002;Montiel et al, 2006;Ghedin et al, 2007;McNulty et al, 2012). Pairwise comparisons between the six Meloidogyne mt genomes showed the lowest divergence levels among the tropical species M. arenaria, M. incognita and M. javanica.…”

Morphological and Mitochondrial Genomic Characterization of Eyeworms (Thelazia callipaeda) from Clinical Cases in Central China

“…Within the large clade, Dracunculidae, Philometridae, and Physalopteridae were in the basal, which was consistent with previous publications (Park et al, 2011; Liu et al, 2013a, 2015). The close relationships among Onchocercidae, Setariidae, and Gnathostomatidae was verified in studies of Park et al (2011); McNulty et al (2012), and Liu et al (2015). In this study, these relationships have also been supported via the addition of more representative sequences.…”

Validation of onchocerciasis biomarker N -acetyltyramine- O -glucuronide (NATOG)

“…Studies have revealed that Wolbachia is necessary for nematode reproduction and survival, plays a central role in nematode pathogenicity, and provides essential metabolic supplementation to their filarial host 23, 24, 25. One major dissimilarity between O. volvulus and L. loa is that O. volvulus is Wolbachia -dependent, whereas L. loa is naturally Wolbachia -free (Fig.4b) 26, 27, 28, 29, 30. In the case of M. perstans , this nematode is host to the supergroup F Wolbachia strain, which is phylogenetically distinct from the supergroup C/D endosymbionts normally present in filarial nematodes including O. volvulus (supergroup C) and L. sigmodontis (supergroup D) 31, 32, 33.…”