Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission
Borrelia burgdorferi (Bb), the causative agent of Lyme disease, adapts to vastly different environments as it cycles between tick vector and vertebrate host. During a tick bloodmeal, Bb alters its gene expression to prepare for vertebrate infection; however, the full range of transcriptional changes...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2023-07-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/86636 |
| _version_ | 1797780523901255680 |
|---|---|
| author | Anne L Sapiro Beth M Hayes Regan F Volk Jenny Y Zhang Diane M Brooks Calla Martyn Atanas Radkov Ziyi Zhao Margie Kinnersley Patrick R Secor Balyn W Zaro Seemay Chou |
| author_facet | Anne L Sapiro Beth M Hayes Regan F Volk Jenny Y Zhang Diane M Brooks Calla Martyn Atanas Radkov Ziyi Zhao Margie Kinnersley Patrick R Secor Balyn W Zaro Seemay Chou |
| author_sort | Anne L Sapiro |
| collection | DOAJ |
| description | Borrelia burgdorferi (Bb), the causative agent of Lyme disease, adapts to vastly different environments as it cycles between tick vector and vertebrate host. During a tick bloodmeal, Bb alters its gene expression to prepare for vertebrate infection; however, the full range of transcriptional changes that occur over several days inside of the tick are technically challenging to capture. We developed an experimental approach to enrich Bb cells to longitudinally define their global transcriptomic landscape inside nymphal Ixodes scapularis ticks during a transmitting bloodmeal. We identified 192 Bb genes that substantially change expression over the course of the bloodmeal from 1 to 4 days after host attachment. The majority of upregulated genes encode proteins found at the cell envelope or proteins of unknown function, including 45 outer surface lipoproteins embedded in the unusual protein-rich coat of Bb. As these proteins may facilitate Bb interactions with the host, we utilized mass spectrometry to identify candidate tick proteins that physically associate with Bb. The Bb enrichment methodology along with the ex vivo Bb transcriptomes and candidate tick interacting proteins presented here provide a resource to facilitate investigations into key determinants of Bb priming and transmission during the tick stage of its unique transmission cycle. |
| first_indexed | 2024-03-12T23:45:17Z |
| format | Article |
| id | doaj.art-3bcf6b0045144e6095c02a956117cc58 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-03-12T23:45:17Z |
| publishDate | 2023-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-3bcf6b0045144e6095c02a956117cc582023-07-14T10:24:50ZengeLife Sciences Publications LtdeLife2050-084X2023-07-011210.7554/eLife.86636Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmissionAnne L Sapiro0https://orcid.org/0000-0002-6612-8272Beth M Hayes1https://orcid.org/0000-0001-6633-751XRegan F Volk2https://orcid.org/0000-0001-6748-719XJenny Y Zhang3https://orcid.org/0000-0003-1352-8018Diane M Brooks4Calla Martyn5Atanas Radkov6Ziyi Zhao7Margie Kinnersley8Patrick R Secor9https://orcid.org/0000-0001-7123-3037Balyn W Zaro10https://orcid.org/0000-0002-8938-9889Seemay Chou11Department of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDepartment of Pharmaceutical Chemistry and Cardiovascular Research Institute, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDivision of Biological Sciences, University of Montana, Missoula, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesDivision of Biological Sciences, University of Montana, Missoula, United StatesDivision of Biological Sciences, University of Montana, Missoula, United StatesDepartment of Pharmaceutical Chemistry and Cardiovascular Research Institute, University of California, San Francisco, San Francisco, United StatesDepartment of Biochemistry & Biophysics, University of California, San Francisco, San Francisco, United StatesBorrelia burgdorferi (Bb), the causative agent of Lyme disease, adapts to vastly different environments as it cycles between tick vector and vertebrate host. During a tick bloodmeal, Bb alters its gene expression to prepare for vertebrate infection; however, the full range of transcriptional changes that occur over several days inside of the tick are technically challenging to capture. We developed an experimental approach to enrich Bb cells to longitudinally define their global transcriptomic landscape inside nymphal Ixodes scapularis ticks during a transmitting bloodmeal. We identified 192 Bb genes that substantially change expression over the course of the bloodmeal from 1 to 4 days after host attachment. The majority of upregulated genes encode proteins found at the cell envelope or proteins of unknown function, including 45 outer surface lipoproteins embedded in the unusual protein-rich coat of Bb. As these proteins may facilitate Bb interactions with the host, we utilized mass spectrometry to identify candidate tick proteins that physically associate with Bb. The Bb enrichment methodology along with the ex vivo Bb transcriptomes and candidate tick interacting proteins presented here provide a resource to facilitate investigations into key determinants of Bb priming and transmission during the tick stage of its unique transmission cycle.https://elifesciences.org/articles/86636Borrelia burgdorferiIxodes scapularisLyme diseaseticksgene expressionhost-microbe interactions |
| spellingShingle | Anne L Sapiro Beth M Hayes Regan F Volk Jenny Y Zhang Diane M Brooks Calla Martyn Atanas Radkov Ziyi Zhao Margie Kinnersley Patrick R Secor Balyn W Zaro Seemay Chou Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission eLife Borrelia burgdorferi Ixodes scapularis Lyme disease ticks gene expression host-microbe interactions |
| title | Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission |
| title_full | Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission |
| title_fullStr | Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission |
| title_full_unstemmed | Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission |
| title_short | Longitudinal map of transcriptome changes in the Lyme pathogen Borrelia burgdorferi during tick-borne transmission |
| title_sort | longitudinal map of transcriptome changes in the lyme pathogen borrelia burgdorferi during tick borne transmission |
| topic | Borrelia burgdorferi Ixodes scapularis Lyme disease ticks gene expression host-microbe interactions |
| url | https://elifesciences.org/articles/86636 |
| work_keys_str_mv | AT annelsapiro longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT bethmhayes longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT reganfvolk longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT jennyyzhang longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT dianembrooks longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT callamartyn longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT atanasradkov longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT ziyizhao longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT margiekinnersley longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT patrickrsecor longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT balynwzaro longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission AT seemaychou longitudinalmapoftranscriptomechangesinthelymepathogenborreliaburgdorferiduringtickbornetransmission |