Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete
Abstract Borrelia burgdorferi, the tick-transmitted spirochete agent of Lyme disease, has a highly segmented genome with a linear chromosome and various linear or circular plasmids. Here, by imaging several chromosomal loci and 16 distinct plasmids, we show that B. burgdorferi is polyploid during gr...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2022-11-01
|
| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-022-34876-4 |
| _version_ | 1827793622533144576 |
|---|---|
| author | Constantin N. Takacs Jenny Wachter Yingjie Xiang Zhongqing Ren Xheni Karaboja Molly Scott Matthew R. Stoner Irnov Irnov Nicholas Jannetty Patricia A. Rosa Xindan Wang Christine Jacobs-Wagner |
| author_facet | Constantin N. Takacs Jenny Wachter Yingjie Xiang Zhongqing Ren Xheni Karaboja Molly Scott Matthew R. Stoner Irnov Irnov Nicholas Jannetty Patricia A. Rosa Xindan Wang Christine Jacobs-Wagner |
| author_sort | Constantin N. Takacs |
| collection | DOAJ |
| description | Abstract Borrelia burgdorferi, the tick-transmitted spirochete agent of Lyme disease, has a highly segmented genome with a linear chromosome and various linear or circular plasmids. Here, by imaging several chromosomal loci and 16 distinct plasmids, we show that B. burgdorferi is polyploid during growth in culture and that the number of genome copies decreases during stationary phase. B. burgdorferi is also polyploid inside fed ticks and chromosome copies are regularly spaced along the spirochete’s length in both growing cultures and ticks. This patterning involves the conserved DNA partitioning protein ParA whose localization is controlled by a potentially phage-derived protein, ParZ, instead of its usual partner ParB. ParZ binds its own coding region and acts as a centromere-binding protein. While ParA works with ParZ, ParB controls the localization of the condensin, SMC. Together, the ParA/ParZ and ParB/SMC pairs ensure faithful chromosome inheritance. Our findings underscore the plasticity of cellular functions, even those as fundamental as chromosome segregation. |
| first_indexed | 2024-03-11T18:21:06Z |
| format | Article |
| id | doaj.art-66f28c58de054aff8c081f7314216b73 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-11T18:21:06Z |
| publishDate | 2022-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-66f28c58de054aff8c081f7314216b732023-10-15T11:20:59ZengNature PortfolioNature Communications2041-17232022-11-0113112210.1038/s41467-022-34876-4Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirocheteConstantin N. Takacs0Jenny Wachter1Yingjie Xiang2Zhongqing Ren3Xheni Karaboja4Molly Scott5Matthew R. Stoner6Irnov Irnov7Nicholas Jannetty8Patricia A. Rosa9Xindan Wang10Christine Jacobs-Wagner11Department of Biology, Stanford UniversityLaboratory of Bacteriology, Rocky Mountain Laboratories, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthDepartment of Mechanical Engineering, Yale UniversityDepartment of Biology, Indiana UniversityDepartment of Biology, Indiana UniversityMicrobial Sciences Institute, Yale West CampusThe Howard Hughes Medical InstituteDepartment of Biology, Stanford UniversityThe Howard Hughes Medical InstituteLaboratory of Bacteriology, Rocky Mountain Laboratories, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of HealthDepartment of Biology, Indiana UniversityDepartment of Biology, Stanford UniversityAbstract Borrelia burgdorferi, the tick-transmitted spirochete agent of Lyme disease, has a highly segmented genome with a linear chromosome and various linear or circular plasmids. Here, by imaging several chromosomal loci and 16 distinct plasmids, we show that B. burgdorferi is polyploid during growth in culture and that the number of genome copies decreases during stationary phase. B. burgdorferi is also polyploid inside fed ticks and chromosome copies are regularly spaced along the spirochete’s length in both growing cultures and ticks. This patterning involves the conserved DNA partitioning protein ParA whose localization is controlled by a potentially phage-derived protein, ParZ, instead of its usual partner ParB. ParZ binds its own coding region and acts as a centromere-binding protein. While ParA works with ParZ, ParB controls the localization of the condensin, SMC. Together, the ParA/ParZ and ParB/SMC pairs ensure faithful chromosome inheritance. Our findings underscore the plasticity of cellular functions, even those as fundamental as chromosome segregation.https://doi.org/10.1038/s41467-022-34876-4 |
| spellingShingle | Constantin N. Takacs Jenny Wachter Yingjie Xiang Zhongqing Ren Xheni Karaboja Molly Scott Matthew R. Stoner Irnov Irnov Nicholas Jannetty Patricia A. Rosa Xindan Wang Christine Jacobs-Wagner Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete Nature Communications |
| title | Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete |
| title_full | Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete |
| title_fullStr | Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete |
| title_full_unstemmed | Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete |
| title_short | Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete |
| title_sort | polyploidy regular patterning of genome copies and unusual control of dna partitioning in the lyme disease spirochete |
| url | https://doi.org/10.1038/s41467-022-34876-4 |
| work_keys_str_mv | AT constantinntakacs polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT jennywachter polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT yingjiexiang polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT zhongqingren polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT xhenikaraboja polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT mollyscott polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT matthewrstoner polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT irnovirnov polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT nicholasjannetty polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT patriciaarosa polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT xindanwang polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete AT christinejacobswagner polyploidyregularpatterningofgenomecopiesandunusualcontrolofdnapartitioninginthelymediseasespirochete |