Metabolic evolution and the self-organization of ecosystems
Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus To understand what drove observed evolutionary patterns, we interpreted them in the conte...
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| Format: | Article |
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National Academy of Sciences (U.S.)
2017
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| Online Access: | http://hdl.handle.net/1721.1/112214 https://orcid.org/0000-0002-4485-8450 https://orcid.org/0000-0002-3102-0341 |
| _version_ | 1826192830720114688 |
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| author | Braakman, Rogier Follows, Michael J Chisholm, Sallie (Penny) |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Braakman, Rogier Follows, Michael J Chisholm, Sallie (Penny) |
| author_sort | Braakman, Rogier |
| collection | MIT |
| description | Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and self-organization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen. |
| first_indexed | 2024-09-23T09:29:50Z |
| format | Article |
| id | mit-1721.1/112214 |
| institution | Massachusetts Institute of Technology |
| last_indexed | 2024-09-23T09:29:50Z |
| publishDate | 2017 |
| publisher | National Academy of Sciences (U.S.) |
| record_format | dspace |
| spelling | mit-1721.1/1122142022-09-26T11:48:05Z Metabolic evolution and the self-organization of ecosystems Braakman, Rogier Follows, Michael J Chisholm, Sallie (Penny) Massachusetts Institute of Technology. Department of Biology Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Braakman, Rogier Follows, Michael J Chisholm, Sallie W Metabolism mediates the flow of matter and energy through the biosphere. We examined how metabolic evolution shapes ecosystems by reconstructing it in the globally abundant oceanic phytoplankter Prochlorococcus To understand what drove observed evolutionary patterns, we interpreted them in the context of its population dynamics, growth rate, and light adaptation, and the size and macromolecular and elemental composition of cells. This multilevel view suggests that, over the course of evolution, there was a steady increase in Prochlorococcus' metabolic rate and excretion of organic carbon. We derived a mathematical framework that suggests these adaptations lower the minimal subsistence nutrient concentration of cells, which results in a drawdown of nutrients in oceanic surface waters. This, in turn, increases total ecosystem biomass and promotes the coevolution of all cells in the ecosystem. Additional reconstructions suggest that Prochlorococcus and the dominant cooccurring heterotrophic bacterium SAR11 form a coevolved mutualism that maximizes their collective metabolic rate by recycling organic carbon through complementary excretion and uptake pathways. Moreover, the metabolic codependencies of Prochlorococcus and SAR11 are highly similar to those of chloroplasts and mitochondria within plant cells. These observations lead us to propose a general theory relating metabolic evolution to the self-amplification and self-organization of the biosphere. We discuss the implications of this framework for the evolution of Earth's biogeochemical cycles and the rise of atmospheric oxygen. Simons Foundation (Grant SCOPE 329108) Gordon and Betty Moore Foundation (Grant 3778) Gordon and Betty Moore Foundation (Grant 495.01) 2017-11-16T21:41:11Z 2017-11-16T21:41:11Z 2017-03 2016-11 2017-10-30T13:42:54Z Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/112214 Braakman, Rogier et al. “Metabolic Evolution and the Self-Organization of Ecosystems.” Proceedings of the National Academy of Sciences 114, 15 (March 2017): E3091–E3100 © 2017 National Academy of Sciences https://orcid.org/0000-0002-4485-8450 https://orcid.org/0000-0002-3102-0341 http://dx.doi.org/10.1073/PNAS.1619573114 Proceedings of the National Academy of Sciences 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 National Academy of Sciences (U.S.) PNAS |
| spellingShingle | Braakman, Rogier Follows, Michael J Chisholm, Sallie (Penny) Metabolic evolution and the self-organization of ecosystems |
| title | Metabolic evolution and the self-organization of ecosystems |
| title_full | Metabolic evolution and the self-organization of ecosystems |
| title_fullStr | Metabolic evolution and the self-organization of ecosystems |
| title_full_unstemmed | Metabolic evolution and the self-organization of ecosystems |
| title_short | Metabolic evolution and the self-organization of ecosystems |
| title_sort | metabolic evolution and the self organization of ecosystems |
| url | http://hdl.handle.net/1721.1/112214 https://orcid.org/0000-0002-4485-8450 https://orcid.org/0000-0002-3102-0341 |
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