Phytoplankton can actively diversify their migration strategy in response to turbulent cues
Marine phytoplankton inhabit a dynamic environment where turbulence, together with nutrient and light availability, shapes species fitness, succession and selection. Many species of phytoplankton are motile and undertake diel vertical migrations to gain access to nutrient-rich deeper layers at night...
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| Format: | Article |
| Language: | en_US |
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Nature Publishing Group
2017
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| Online Access: | http://hdl.handle.net/1721.1/111154 https://orcid.org/0000-0001-5592-7864 https://orcid.org/0000-0003-2827-5615 https://orcid.org/0000-0002-3199-0508 |
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| author | Sengupta, Anupam Carrara, Francesco Stocker, Roman |
| author2 | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Sengupta, Anupam Carrara, Francesco Stocker, Roman |
| author_sort | Sengupta, Anupam |
| collection | MIT |
| description | Marine phytoplankton inhabit a dynamic environment where turbulence, together with nutrient and light availability, shapes species fitness, succession and selection. Many species of phytoplankton are motile and undertake diel vertical migrations to gain access to nutrient-rich deeper layers at night and well-lit surface waters during the day. Disruption of this migratory strategy by turbulence is considered to be an important cause of the succession between motile and non-motile species when conditions turn turbulent. However, this classical view neglects the possibility that motile species may actively respond to turbulent cues to avoid layers of strong turbulence. Here we report that phytoplankton, including raphidophytes and dinoflagellates, can actively diversify their migratory strategy in response to hydrodynamic cues characteristic of overturning by Kolmogorov-scale eddies. Upon experiencing repeated overturning with timescales and statistics representative of ocean turbulence, an upward-swimming population rapidly (5–60 min) splits into two subpopulations, one swimming upward and one swimming downward. Quantitative morphological analysis of the harmful-algal-bloom-forming raphidophyte Heterosigma akashiwo together with a model of cell mechanics revealed that this behaviour was accompanied by a modulation of the cells’ fore–aft asymmetry. The minute magnitude of the required modulation, sufficient to invert the preferential swimming direction of the cells, highlights the advanced level of control that phytoplankton can exert on their migratory behaviour. Together with observations of enhanced cellular stress after overturning and the typically deleterious effects of strong turbulence on motile phytoplankton these results point to an active adaptation of H. akashiwo to increase the chance of evading turbulent layers by diversifying the direction of migration within the population, in a manner suggestive of evolutionary bet-hedging. This migratory behaviour relaxes the boundaries between the fluid dynamic niches of motile and non-motile phytoplankton, and highlights that rapid responses to hydrodynamic cues are important survival strategies for phytoplankton in the ocean. |
| first_indexed | 2024-09-23T09:34:03Z |
| format | Article |
| id | mit-1721.1/111154 |
| institution | Massachusetts Institute of Technology |
| language | en_US |
| last_indexed | 2024-09-23T09:34:03Z |
| publishDate | 2017 |
| publisher | Nature Publishing Group |
| record_format | dspace |
| spelling | mit-1721.1/1111542024-06-28T14:42:58Z Phytoplankton can actively diversify their migration strategy in response to turbulent cues Sengupta, Anupam Carrara, Francesco Stocker, Roman Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Parsons Laboratory for Environmental Science and Engineering (Massachusetts Institute of Technology) Sengupta, Anupam Carrara, Francesco Stocker, Roman Marine phytoplankton inhabit a dynamic environment where turbulence, together with nutrient and light availability, shapes species fitness, succession and selection. Many species of phytoplankton are motile and undertake diel vertical migrations to gain access to nutrient-rich deeper layers at night and well-lit surface waters during the day. Disruption of this migratory strategy by turbulence is considered to be an important cause of the succession between motile and non-motile species when conditions turn turbulent. However, this classical view neglects the possibility that motile species may actively respond to turbulent cues to avoid layers of strong turbulence. Here we report that phytoplankton, including raphidophytes and dinoflagellates, can actively diversify their migratory strategy in response to hydrodynamic cues characteristic of overturning by Kolmogorov-scale eddies. Upon experiencing repeated overturning with timescales and statistics representative of ocean turbulence, an upward-swimming population rapidly (5–60 min) splits into two subpopulations, one swimming upward and one swimming downward. Quantitative morphological analysis of the harmful-algal-bloom-forming raphidophyte Heterosigma akashiwo together with a model of cell mechanics revealed that this behaviour was accompanied by a modulation of the cells’ fore–aft asymmetry. The minute magnitude of the required modulation, sufficient to invert the preferential swimming direction of the cells, highlights the advanced level of control that phytoplankton can exert on their migratory behaviour. Together with observations of enhanced cellular stress after overturning and the typically deleterious effects of strong turbulence on motile phytoplankton these results point to an active adaptation of H. akashiwo to increase the chance of evading turbulent layers by diversifying the direction of migration within the population, in a manner suggestive of evolutionary bet-hedging. This migratory behaviour relaxes the boundaries between the fluid dynamic niches of motile and non-motile phytoplankton, and highlights that rapid responses to hydrodynamic cues are important survival strategies for phytoplankton in the ocean. Gordon and Betty Moore Foundation (Award GBMF 3783) 2017-09-07T18:03:22Z 2017-09-07T18:03:22Z 2017-03 2016-07 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/111154 Sengupta, Anupam et al. “Phytoplankton Can Actively Diversify Their Migration Strategy in Response to Turbulent Cues.” Nature 543, 7646 (March 2017): 555–558 © 2017 Nature Publishing Group https://orcid.org/0000-0001-5592-7864 https://orcid.org/0000-0003-2827-5615 https://orcid.org/0000-0002-3199-0508 en_US http://dx.doi.org/10.1038/nature21415 Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Nature Publishing Group Prof. Stocker |
| spellingShingle | Sengupta, Anupam Carrara, Francesco Stocker, Roman Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title | Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title_full | Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title_fullStr | Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title_full_unstemmed | Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title_short | Phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| title_sort | phytoplankton can actively diversify their migration strategy in response to turbulent cues |
| url | http://hdl.handle.net/1721.1/111154 https://orcid.org/0000-0001-5592-7864 https://orcid.org/0000-0003-2827-5615 https://orcid.org/0000-0002-3199-0508 |
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