Abstract
BackgroundFleas (Insecta: Siphonaptera) are small flightless parasites of birds and mammals; their blood-feeding can transmit many serious pathogens (i.e., the etiological agents of bubonic plague, endemic and murine typhus). The lack of flea genome assemblies has hindered research, especially comparisons to other disease vectors. Accordingly, we sequenced the genome of the cat flea, Ctenocephalides felis, an insect with substantial human health and veterinary importance across the globe.ResultsBy combining Illumina and PacBio sequencing of DNA derived from multiple inbred female fleas with Hi-C scaffolding techniques, we generated a chromosome-level genome assembly for C. felis. Unexpectedly, our assembly revealed extensive gene duplication across the entire genome, exemplified by ~ 38% of protein-coding genes with two or more copies and over 4000 tRNA genes. A broad range of genome size determinations (433–551 Mb) for individual fleas sampled across different populations supports the widespread presence of fluctuating copy number variation (CNV) in C. felis. Similarly, broad genome sizes were also calculated for individuals of Xenopsylla cheopis (Oriental rat flea), indicating that this remarkable “genome-in-flux” phenomenon could be a siphonapteran-wide trait. Finally, from the C. felis sequence reads, we also generated closed genomes for two novel strains of Wolbachia, one parasitic and one symbiotic, found to co-infect individual fleas.ConclusionRampant CNV in C. felis has dire implications for gene-targeting pest control measures and stands to complicate standard normalization procedures utilized in comparative transcriptomics analysis. Coupled with co-infection by novel Wolbachia endosymbionts—potential tools for blocking pathogen transmission—these oddities highlight a unique and underappreciated disease vector.
Highlights
Fleas (Insecta: Siphonaptera) are small flightless parasites of birds and mammals; their blood-feeding can transmit many serious pathogens
Distances were computed only for true duplications (n = 2 genes) at a threshold of 90% aa identity. d Gene duplications are enriched within BIG9 scaffolds versus across scaffolds. e Enriched cellular functions of duplicate genes relative to single-copy genes. f C. felis belongs to a minimal fraction of eukaryotes containing abundant tRNA genes. tRNA gene counts are shown for disease vectors (VectorBase [26]) and eukaryotes carrying over 1000 tRNA genes (GtRNAdb [27]); ratios show the number of genomes with > 1000 tRNA genes per taxon we focus our subsequent analyses on the BIG9 scaffolds unless otherwise noted
Since transposons and other repeat elements are relatively sparse in C. felis and cannot account for such rampant copy number variation (CNV), and given that no individual flea genome size was estimated to be larger than our BIG9 assembly, we posit that unequal crossing over and gene conversion continually create and eliminate large linear stretches of DNA to keep the C. felis genome in a fluctuating continuum
Summary
Fleas (Insecta: Siphonaptera) are small flightless parasites of birds and mammals; their blood-feeding can transmit many serious pathogens (i.e., the etiological agents of bubonic plague, endemic and murine typhus). We sequenced the genome of the cat flea, Ctenocephalides felis, an insect with substantial human health and veterinary importance across the globe. Fleas that feed away from their primary hosts (black rats and other murids) can introduce Y. pestis to humans, which historically has eliminated a substantial fraction of the world’s human population, e.g., the Plague of Justinian and the Black Death [5]. Bubonic plague remains a significant threat to human health [6, 7] as do other noteworthy diseases propagated by flea infestations, including murine typhus (Rickettsia typhi), murine typhus-like illness (R. felis), cat-scratch disease (Bartonella henselae), and myxomatosis (Myxoma virus) [8, 9]. Fleas inflict a multifaceted human health burden with enormous public health relevance [13]
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