Mitochondrial genomes ofColumbicolafeather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice

Abstract

Most animals have a conserved mitochondrial genome structure composed of a single chromosome. However, some organisms have their mitochondrial genes separated on several smaller circular or linear chromosomes. Highly fragmented circular chromosomes ("minicircles") are especially prevalent in parasitic lice (Insecta: Phthiraptera), with 16 species known to have between 9 and 20 mitochondrial minicircles per genome. All of these species belong to the same clade (mammalian lice), suggesting a single origin of drastic fragmentation.Nevertheless, other work indicates a lesser degree of fragmentation (2-3 chromosomes/genome) is present in some avian feather lice (Ischnocera: Philopteridae). In this study, we tested for minicircles in four species of the feather louse genus Columbicola (Philopteridae). Using whole genome shotgun sequence data, we applied three different bioinformatic approaches for assembling the Columbicola mitochondrial genome. We further confirmed these approaches by assembling the mitochondrial genome of Pediculus humanus from shotgun sequencing reads, a species known to have minicircles. All three methods indicated Columbicola spp. genomes are highly fragmented into 15-17 minicircles between 1,119 and 3,173 bp in length, with 1-4 genes per minicircle. Subsequent annotation of the minicircles indicated that tRNA arrangements of minicircles varied substantially between species. These mitochondrial minicircles for species of Columbicola represent the first feather lice (Philopteridae) for which minicircles have been found in a full mitochondrial genome assembly. Combined with recent phylogenetic studies of parasitic lice, our results provide strong evidence that highly fragmented mitochondrial genomes, which are otherwise rare across the Tree of Life, evolved multiple times within parasitic lice.

Highly Rearranged Mitochondrial Genome in Falcolipeurus lice (Phthiraptera: Philopteridae) from Endangered Eagles

“…Previous studies of other lice have detected high level difference in protein sequences. For example, difference in amino acid sequences of the 13 protein-coding genes between C. picui and C. cruziana was 5.5-50% [16], and C. bidentatus compar and C. compar was 0-37.3% [11,14]. Taken together, the molecular evidence presented here supports that F. suturalis and F. quadripustulatus represent distinct louse species.…”

“…The Philopteridae is a large family within the suborder Ischnocera [12], but the complete mt genomes of only a limited number of species have been sequenced, including Bothriometopus macrocnemis [13], Campanulotes bidentatus compar [14], Campanulotes compar [11], Coloceras sp. SLC-2011 [15], Falcolipeurus quadripustulatus [11], Ibidoecus bisignatus [15], Columbina picui, Columbina cruziana, Columbicola columbae [16]. These results showed extensive gene rearrangements in their mt genomes.…”

“…These results showed extensive gene rearrangements in their mt genomes. Very surprisingly, a recently report has demonstrated that highly-fragmented, mt minicircles are present in four species of the genus Columbicola within the Philopteridae [16], indicated fragmented mt genomes are more prevalent in parasitic lice than previously assumed [11]. However, our knowledge on the structure of mt genomes of bird lice from this family is far from comprehensive.…”

A novel fragmented mitochondrial genome in the protist pathogenToxoplasma gondiiand related tissue coccidia

“…However, increasing bodies of literature indicate that this structure is 39 not universal and that considerable evolution of both genome structure and gene content 40 has occurred in both protists and multicellular eukaryotes ; Gissi et al 41 of angiosperms ranges from 200 kb to 11 Mb in size and shows a huge variation in 48 structure, content, gene/DNA transfers and processes such as RNA editing (Gualberto and 49 Newton 2017; Petersen et al 2017). Mitochondrial genomes consisting of multiple 50 divergent circular molecules have been noted in the fungus Spizellomyces (Burger and 51 Lang 2003), Columbicola feather lice (Sweet et al 2019) and certain cnidarian parasites 52 (Yahalomi et al 2017). Among the protists, the kinetoplastid mtDNA (called kDNA) 53 consists of multiple gene-encoding maxi-circles and guide RNA encoding minicircles that 54 form a tight physical network, the kinetoplast (Morris et al 2001).…”

A novel fragmented mitochondrial genome in the protist pathogen Toxoplasma gondii and related tissue coccidia

“…At the other end of the size spectrum, the mtDNA of angiosperms ranges from 200 kb to 11 Mb in size and shows a huge variation in structure, content, gene/DNA transfers, and processes such as RNA editing (Gualberto and Newton 2017). Mitochondrial genomes consisting of multiple divergent circular molecules have been noted in the fungus Spizellomyces , Columbicola feather lice (Sweet et al 2020), and certain cnidarian parasites (Yahalomi et al 2017). Among the protists, the kinetoplastid mtDNA (called kDNA) consists of multiple gene-encoding maxicircles and guide RNA encoding minicircles that form a tight physical network, the kinetoplast (Morris et al 2001).…”