A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity
Abstract Background 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). The lack of flea genome assemblies has hindered research, especi...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2020-06-01
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| Series: | BMC Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12915-020-00802-7 |
| _version_ | 1818136546681815040 |
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| author | Timothy P. Driscoll Victoria I. Verhoeve Joseph J. Gillespie J. Spencer Johnston Mark L. Guillotte Kristen E. Rennoll-Bankert M. Sayeedur Rahman Darren Hagen Christine G. Elsik Kevin R. Macaluso Abdu F. Azad |
| author_facet | Timothy P. Driscoll Victoria I. Verhoeve Joseph J. Gillespie J. Spencer Johnston Mark L. Guillotte Kristen E. Rennoll-Bankert M. Sayeedur Rahman Darren Hagen Christine G. Elsik Kevin R. Macaluso Abdu F. Azad |
| author_sort | Timothy P. Driscoll |
| collection | DOAJ |
| description | Abstract Background 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). 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. Results By 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. Conclusion Rampant 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. |
| first_indexed | 2024-12-11T09:42:08Z |
| format | Article |
| id | doaj.art-65f7da03c7cb4e78addaea291ae4f199 |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-11T09:42:08Z |
| publishDate | 2020-06-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-65f7da03c7cb4e78addaea291ae4f1992022-12-22T01:12:38ZengBMCBMC Biology1741-70072020-06-0118111910.1186/s12915-020-00802-7A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticityTimothy P. Driscoll0Victoria I. Verhoeve1Joseph J. Gillespie2J. Spencer Johnston3Mark L. Guillotte4Kristen E. Rennoll-Bankert5M. Sayeedur Rahman6Darren Hagen7Christine G. Elsik8Kevin R. Macaluso9Abdu F. Azad10Department of Biology, West Virginia UniversityDepartment of Microbiology and Immunology, University of Maryland School of MedicineDepartment of Microbiology and Immunology, University of Maryland School of MedicineDepartment of Entomology, Texas A&M UniversityDepartment of Microbiology and Immunology, University of Maryland School of MedicineDepartment of Microbiology and Immunology, University of Maryland School of MedicineDepartment of Microbiology and Immunology, University of Maryland School of MedicineDepartment of Animal and Food Sciences, Oklahoma State UniversityDivision of Animal Sciences, University of MissouriDepartment of Microbiology and Immunology, College of Medicine, University of South AlabamaDepartment of Microbiology and Immunology, University of Maryland School of MedicineAbstract Background 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). 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. Results By 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. Conclusion Rampant 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.http://link.springer.com/article/10.1186/s12915-020-00802-7Ctenocephalides felisCat fleaGenomeHi-C assemblyPacBio sequencingWolbachia |
| spellingShingle | Timothy P. Driscoll Victoria I. Verhoeve Joseph J. Gillespie J. Spencer Johnston Mark L. Guillotte Kristen E. Rennoll-Bankert M. Sayeedur Rahman Darren Hagen Christine G. Elsik Kevin R. Macaluso Abdu F. Azad A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity BMC Biology Ctenocephalides felis Cat flea Genome Hi-C assembly PacBio sequencing Wolbachia |
| title | A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| title_full | A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| title_fullStr | A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| title_full_unstemmed | A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| title_short | A chromosome-level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| title_sort | chromosome level assembly of the cat flea genome uncovers rampant gene duplication and genome size plasticity |
| topic | Ctenocephalides felis Cat flea Genome Hi-C assembly PacBio sequencing Wolbachia |
| url | http://link.springer.com/article/10.1186/s12915-020-00802-7 |
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