Co-culture and biogeography of Prochlorococcus and SAR11
Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describ...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Springer Science and Business Media LLC
2020
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| Online Access: | https://hdl.handle.net/1721.1/125545 |
| _version_ | 1811091149834682368 |
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| author | Becker, Jamie William Hogle, Shane Lahman Rosendo, Kali M Chisholm, Sallie (Penny) |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Becker, Jamie William Hogle, Shane Lahman Rosendo, Kali M Chisholm, Sallie (Penny) |
| author_sort | Becker, Jamie William |
| collection | MIT |
| description | Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups. |
| first_indexed | 2024-09-23T14:57:47Z |
| format | Article |
| id | mit-1721.1/125545 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T14:57:47Z |
| publishDate | 2020 |
| publisher | Springer Science and Business Media LLC |
| record_format | dspace |
| spelling | mit-1721.1/1255452022-09-29T11:44:01Z Co-culture and biogeography of Prochlorococcus and SAR11 Becker, Jamie William Hogle, Shane Lahman Rosendo, Kali M Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups. National Science Foundation (U.S.). (Grant DBI-0424599) National Science Foundation (U.S.) (Grant OCE-1153588) Simons Foundation (Life Sciences Project Award ID 337262, SCOPE award ID 329108) Gordon and Betty Moore Foundation (Grant IDs GBMF495 and GBMF4511) 2020-05-28T15:16:15Z 2020-05-28T15:16:15Z 2019-02 2019-01 2020-05-20T18:47:38Z Article http://purl.org/eprint/type/JournalArticle 1751-7362 1751-7370 https://hdl.handle.net/1721.1/125545 Becker, Jamie W., et al. "Co-culture and biogeography of Prochlorococcus and SAR11." The ISME Journal (2019) 13:1506–1519 © 2019, The Author(s). en https://dx.doi.org/10.1038/S41396-019-0365-4 ISME Journal Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Springer Science and Business Media LLC ISME Journal |
| spellingShingle | Becker, Jamie William Hogle, Shane Lahman Rosendo, Kali M Chisholm, Sallie (Penny) Co-culture and biogeography of Prochlorococcus and SAR11 |
| title | Co-culture and biogeography of Prochlorococcus and SAR11 |
| title_full | Co-culture and biogeography of Prochlorococcus and SAR11 |
| title_fullStr | Co-culture and biogeography of Prochlorococcus and SAR11 |
| title_full_unstemmed | Co-culture and biogeography of Prochlorococcus and SAR11 |
| title_short | Co-culture and biogeography of Prochlorococcus and SAR11 |
| title_sort | co culture and biogeography of prochlorococcus and sar11 |
| url | https://hdl.handle.net/1721.1/125545 |
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