Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems
Abstract Background Bartonella are intracellular bacteria that are transmitted via animal scratches, bites and hematophagous arthropods. Rodents and their associated fleas play a key role in the maintenance of Bartonella worldwide, with > 22 species identified in rodent hosts. No studies have add...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-10-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-022-05446-w |
| _version_ | 1798029975215931392 |
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| author | Kayla J. Buhler Champika Fernando Janet E. Hill Terry Galloway Suzanne Carriere Heather Fenton Dominique Fauteux Emily J. Jenkins |
| author_facet | Kayla J. Buhler Champika Fernando Janet E. Hill Terry Galloway Suzanne Carriere Heather Fenton Dominique Fauteux Emily J. Jenkins |
| author_sort | Kayla J. Buhler |
| collection | DOAJ |
| description | Abstract Background Bartonella are intracellular bacteria that are transmitted via animal scratches, bites and hematophagous arthropods. Rodents and their associated fleas play a key role in the maintenance of Bartonella worldwide, with > 22 species identified in rodent hosts. No studies have addressed the occurrence and diversity of Bartonella species and vectors for small mammals in Arctic and Subarctic ecosystems, which are increasingly impacted by invasive species and climate change. Methods In this study, we characterized the diversity of rodent fleas using conventional PCR targeting the mitochondrial cytochrome c oxidase II gene (COII) and Bartonella species in rodents and shrews (n = 505) from northern Canada using conventional PCR targeting the ITS (intergenic transcribed spacer) region and gltA (citrate synthase) gene. Metagenomic sequencing of a portion of the gltA gene was completed on a subset of 42 rodents and four rodent flea pools. Results Year, total summer precipitation the year prior to sampling, average minimum spring temperature and small mammal species were significant factors in predicting Bartonella positivity. Occurrence based on the ITS region was more than double that of the gltA gene and was 34% (n = 349) in northern red-backed voles, 35% (n = 20) in meadow voles, 37% (n = 68) in deer mice and 31% (n = 59) in shrews. Six species of Bartonella were identified with the ITS region, including B. grahamii, B. elizabethae, B. washoensis, Candidatus B. rudakovii, B. doshiae, B. vinsonii subsp. berkhoffii and subsp. arupensis. In addition, 47% (n = 49/105) of ITS amplicons had < 97% identity to sequences in GenBank, possibly due to a limited reference library or previously unreported species. An additional Bartonella species (B. heixiaziensis) was detected during metagenomic sequencing of the gltA gene in 6/11 rodents that had ITS sequences with < 97% identity in GenBank, highlighting that a limited reference library for the ITS marker likely accounted for low sequence similarity in our specimens. In addition, one flea pool from a northern red-backed vole contained multiple species (B. grahamii and B. heixiaziensis). Conclusion Our study calls attention to the usefulness of a combined approach to determine the occurrence and diversity of Bartonella communities in hosts and vectors. Graphical Abstract |
| first_indexed | 2024-04-11T19:32:56Z |
| format | Article |
| id | doaj.art-69d0a0e76a654e4f87837a37ee57fdc5 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-04-11T19:32:56Z |
| publishDate | 2022-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-69d0a0e76a654e4f87837a37ee57fdc52022-12-22T04:06:56ZengBMCParasites & Vectors1756-33052022-10-0115111410.1186/s13071-022-05446-wCombining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystemsKayla J. Buhler0Champika Fernando1Janet E. Hill2Terry Galloway3Suzanne Carriere4Heather Fenton5Dominique Fauteux6Emily J. Jenkins7Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of SaskatchewanDepartment of Veterinary Microbiology, Western College of Veterinary Medicine, University of SaskatchewanDepartment of Veterinary Microbiology, Western College of Veterinary Medicine, University of SaskatchewanDepartment of Entomology, Faculty of Agricultural and Food Sciences, University of ManitobaDepartment of Environment and Natural Resources, 5Th Floor Scotiabank Centre, Government of The Northwest TerritoriesDepartment of Environment and Natural Resources, 5Th Floor Scotiabank Centre, Government of The Northwest TerritoriesCentre for Arctic Knowledge and Exploration, Canadian Museum of NatureDepartment of Veterinary Microbiology, Western College of Veterinary Medicine, University of SaskatchewanAbstract Background Bartonella are intracellular bacteria that are transmitted via animal scratches, bites and hematophagous arthropods. Rodents and their associated fleas play a key role in the maintenance of Bartonella worldwide, with > 22 species identified in rodent hosts. No studies have addressed the occurrence and diversity of Bartonella species and vectors for small mammals in Arctic and Subarctic ecosystems, which are increasingly impacted by invasive species and climate change. Methods In this study, we characterized the diversity of rodent fleas using conventional PCR targeting the mitochondrial cytochrome c oxidase II gene (COII) and Bartonella species in rodents and shrews (n = 505) from northern Canada using conventional PCR targeting the ITS (intergenic transcribed spacer) region and gltA (citrate synthase) gene. Metagenomic sequencing of a portion of the gltA gene was completed on a subset of 42 rodents and four rodent flea pools. Results Year, total summer precipitation the year prior to sampling, average minimum spring temperature and small mammal species were significant factors in predicting Bartonella positivity. Occurrence based on the ITS region was more than double that of the gltA gene and was 34% (n = 349) in northern red-backed voles, 35% (n = 20) in meadow voles, 37% (n = 68) in deer mice and 31% (n = 59) in shrews. Six species of Bartonella were identified with the ITS region, including B. grahamii, B. elizabethae, B. washoensis, Candidatus B. rudakovii, B. doshiae, B. vinsonii subsp. berkhoffii and subsp. arupensis. In addition, 47% (n = 49/105) of ITS amplicons had < 97% identity to sequences in GenBank, possibly due to a limited reference library or previously unreported species. An additional Bartonella species (B. heixiaziensis) was detected during metagenomic sequencing of the gltA gene in 6/11 rodents that had ITS sequences with < 97% identity in GenBank, highlighting that a limited reference library for the ITS marker likely accounted for low sequence similarity in our specimens. In addition, one flea pool from a northern red-backed vole contained multiple species (B. grahamii and B. heixiaziensis). Conclusion Our study calls attention to the usefulness of a combined approach to determine the occurrence and diversity of Bartonella communities in hosts and vectors. Graphical Abstracthttps://doi.org/10.1186/s13071-022-05446-wZoonosesBartonellaVector-borne diseaseFleasRodentsArctic |
| spellingShingle | Kayla J. Buhler Champika Fernando Janet E. Hill Terry Galloway Suzanne Carriere Heather Fenton Dominique Fauteux Emily J. Jenkins Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems Parasites & Vectors Zoonoses Bartonella Vector-borne disease Fleas Rodents Arctic |
| title | Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems |
| title_full | Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems |
| title_fullStr | Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems |
| title_full_unstemmed | Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems |
| title_short | Combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and Bartonella in rodents and shrews from Arctic and Subarctic ecosystems |
| title_sort | combining deep sequencing and conventional molecular approaches reveals broad diversity and distribution of fleas and bartonella in rodents and shrews from arctic and subarctic ecosystems |
| topic | Zoonoses Bartonella Vector-borne disease Fleas Rodents Arctic |
| url | https://doi.org/10.1186/s13071-022-05446-w |
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