Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation
The picocyanobacteria Prochlorococcus and Synechococcus are found throughout the ocean's euphotic zone, where the daily light:dark cycle drives their physiology. Periodic deep mixing events can, however, move cells below this region, depriving them of light for extended periods of time. Here, w...
| Main Authors: | , , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Article |
| Language: | English |
| Published: |
Wiley
2021
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| Online Access: | https://hdl.handle.net/1721.1/132776 |
| _version_ | 1811095625600598016 |
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| author | Coe, Allison Biller, Steven J Thomas, Elaina Boulias, Konstantinos Bliem, Christina Arellano, Aldo Dooley, Keven Rasmussen, Anna N LeGault, Kristen O'Keefe, Tyler J Stover, Sarah Greer, Eric L Chisholm, Sallie W |
| author2 | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Coe, Allison Biller, Steven J Thomas, Elaina Boulias, Konstantinos Bliem, Christina Arellano, Aldo Dooley, Keven Rasmussen, Anna N LeGault, Kristen O'Keefe, Tyler J Stover, Sarah Greer, Eric L Chisholm, Sallie W |
| author_sort | Coe, Allison |
| collection | MIT |
| description | The picocyanobacteria Prochlorococcus and Synechococcus are found throughout the ocean's euphotic zone, where the daily light:dark cycle drives their physiology. Periodic deep mixing events can, however, move cells below this region, depriving them of light for extended periods of time. Here, we demonstrate that members of these genera can adapt to tolerate repeated periods of light energy deprivation. Strains kept in the dark for 3 d and then returned to the light initially required 18–26 d to resume growth, but after multiple rounds of dark exposure they began to regrow after only 1–2 d. This dark-tolerant phenotype was stable and heritable; some cultures retained the trait for over 132 generations even when grown in a standard 13:11 light:dark cycle. We found no genetic differences between the dark-tolerant and parental strains of Prochlorococcus NATL2A, indicating that an epigenetic change is likely responsible for the adaptation. To begin to explore this possibility, we asked whether DNA methylation—one potential mechanism mediating epigenetic inheritance in bacteria—occurs in Prochlorococcus. LC–MS/MS analysis showed that while DNA methylations, including 6 mA and 5 mC, are found in some other Prochlorococcus strains, there were no methylations detected in either the parental or dark-tolerant NATL2A strains. These findings suggest that Prochlorococcus utilizes a yet-to-be-determined epigenetic mechanism to adapt to the stress of extended light energy deprivation, and highlights phenotypic heterogeneity as an additional dimension of Prochlorococcus diversity. |
| first_indexed | 2024-09-23T16:21:39Z |
| format | Article |
| id | mit-1721.1/132776 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T16:21:39Z |
| publishDate | 2021 |
| publisher | Wiley |
| record_format | dspace |
| spelling | mit-1721.1/1327762024-06-03T17:14:27Z Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation Coe, Allison Biller, Steven J Thomas, Elaina Boulias, Konstantinos Bliem, Christina Arellano, Aldo Dooley, Keven Rasmussen, Anna N LeGault, Kristen O'Keefe, Tyler J Stover, Sarah Greer, Eric L Chisholm, Sallie W Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Massachusetts Institute of Technology. Department of Biology The picocyanobacteria Prochlorococcus and Synechococcus are found throughout the ocean's euphotic zone, where the daily light:dark cycle drives their physiology. Periodic deep mixing events can, however, move cells below this region, depriving them of light for extended periods of time. Here, we demonstrate that members of these genera can adapt to tolerate repeated periods of light energy deprivation. Strains kept in the dark for 3 d and then returned to the light initially required 18–26 d to resume growth, but after multiple rounds of dark exposure they began to regrow after only 1–2 d. This dark-tolerant phenotype was stable and heritable; some cultures retained the trait for over 132 generations even when grown in a standard 13:11 light:dark cycle. We found no genetic differences between the dark-tolerant and parental strains of Prochlorococcus NATL2A, indicating that an epigenetic change is likely responsible for the adaptation. To begin to explore this possibility, we asked whether DNA methylation—one potential mechanism mediating epigenetic inheritance in bacteria—occurs in Prochlorococcus. LC–MS/MS analysis showed that while DNA methylations, including 6 mA and 5 mC, are found in some other Prochlorococcus strains, there were no methylations detected in either the parental or dark-tolerant NATL2A strains. These findings suggest that Prochlorococcus utilizes a yet-to-be-determined epigenetic mechanism to adapt to the stress of extended light energy deprivation, and highlights phenotypic heterogeneity as an additional dimension of Prochlorococcus diversity. 2021-10-07T15:16:40Z 2021-10-07T15:16:40Z 2021-09 2021-03 2021-10-06T14:47:28Z Article http://purl.org/eprint/type/JournalArticle 1939-5590 https://hdl.handle.net/1721.1/132776 Coe, A., Biller, S.J., Thomas, E., Boulias, K., Bliem, C., Arellano, A., Dooley, K., Rasmussen, A.N., LeGault, K., O'Keefe, T.J., Stover, S., Greer, E.L. and Chisholm, S.W. (2021), Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation. Limnol Oceanogr, 66: 3300-3312 en 10.1002/lno.11880 Limnology and Oceanography Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Wiley Wiley |
| spellingShingle | Coe, Allison Biller, Steven J Thomas, Elaina Boulias, Konstantinos Bliem, Christina Arellano, Aldo Dooley, Keven Rasmussen, Anna N LeGault, Kristen O'Keefe, Tyler J Stover, Sarah Greer, Eric L Chisholm, Sallie W Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title | Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title_full | Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title_fullStr | Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title_full_unstemmed | Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title_short | Coping with darkness: The adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| title_sort | coping with darkness the adaptive response of marine picocyanobacteria to repeated light energy deprivation |
| url | https://hdl.handle.net/1721.1/132776 |
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