Genome skimming reveals a multipartite mitochondrial genome in the parasitic nematode Dioctophyme renale

Abstract

Background Dioctophyme renale, known as the “giant kidney worm,” is a parasitic nematode of significant medical and biological importance due to its large size and complex interactions with various mammals, including humans, causing dioctophymiasis. Despite its importance, genomic information for D. renale is limited. Only partial sequences of mitochondrial genes and 18S rRNA have been reported, classifying it within Clade I nematodes, alongside Trichuris and Trichinella. Mitochondrial genomes are valuable for phylogenetic, biogeographic, and population studies. The nematode mitochondrial genome is typically circular, encoding 12 protein-coding genes, 22 tRNAs, and two rRNAs, although some species exhibit multipartite mitogenomes. Given the lack of comprehensive genomic data, this study aims to sequence the mitogenome of D. renale using genome skimming and long-read sequencing, and to perform comparative analyses to assess its structure, composition, and phylogenetic relationships within Clade I nematodes, considering the influence of its unique life history traits. Results We found that the single circular mitochondrial chromosome typically found in animals has evolved into a multipartite organization in Dioctophyme renale, consisting of eleven minichromosomes, each containing a single protein-coding gene and an associated non-coding region. While multipartite mitogenomes have been reported in other metazoan lineages, this architecture, strongly supported by long-read sequencing from independent library constructions, represents a novel mitogenome structure within nematodes. Comparative analyses indicate that mitochondrial protein-coding sequences in D. renale cluster phylogenetically with those of vertebrate-parasitic nematodes within Clade I, whereas the structural fragmentation of the mitogenome appears to have evolved independently. Conclusions Although the functional implications of a multipartite mitogenome remain unknown, future work should examine whether specific life-history traits or selective pressures associated with parasitism may have contributed to its emergence. We also present a long-read genome-skimming workflow suitable for non-model organisms, offering a strategy to expand mitogenomic resources in taxonomic groups that remain markedly underrepresented.