A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum
Symbiotic interactions drive species evolution, with nutritional symbioses playing vital roles across ecosystems. Chemosynthetic symbioses are globally distributed and ecologically significant, yet the lack of model systems has hindered research progress. The giant ciliate Zoothamnium niveum and its...
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Frontiers Media S.A.
2024-12-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491485/full |
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| author | P. E. Contarini E. Emboule P. Jean-Louis T. Woyke S. V. Date O. Gros J-M. Volland J-M. Volland J-M. Volland |
| author_facet | P. E. Contarini E. Emboule P. Jean-Louis T. Woyke S. V. Date O. Gros J-M. Volland J-M. Volland J-M. Volland |
| author_sort | P. E. Contarini |
| collection | DOAJ |
| description | Symbiotic interactions drive species evolution, with nutritional symbioses playing vital roles across ecosystems. Chemosynthetic symbioses are globally distributed and ecologically significant, yet the lack of model systems has hindered research progress. The giant ciliate Zoothamnium niveum and its sulfur-oxidizing symbionts represent the only known chemosynthetic symbiosis with a short life span that has been transiently cultivated in the laboratory. While it is experimentally tractable and presents a promising model system, it currently lacks an open-source, simple, and standardized cultivation setup. Following the FABricated Ecosystems (EcoFABs) model, we leveraged 3D printing and polydimethylsiloxane (PDMS) casting to develop simple flow-through cultivation chambers that can be produced and adopted by any laboratory. The streamlined manufacturing process reduces production time by 86% and cuts cost by tenfold compared to the previous system. Benchmarking using previously established optimal growth conditions, the new open-source cultivation system proves stable, efficient, more autonomous, and promotes a more prolific growth of the symbiosis. For the first time, starting from single cells, we successfully cultivated the symbiosis in flow-through chambers for 20 days, spanning multiple generations of colonies that remained symbiotic. They were transferred from chamber to chamber enabling long-term cultivation and eliminating the need for continuous field sampling. The chambers, optimized for live imaging, allowed detailed observation of the synchronized growth between the host and symbiont. Highlighting the benefit of this new system, we here describe a new step in the first hours of development where the host pauses growth, expels a coat, before resuming growth, hinting at a putative symbiont selection mechanism early in the colony life cycle. With this simple, open-source, cultivation setup, Z. niveum holds promises for comparative studies, standardization of research and wide adoption by the symbiosis research community. |
| format | Article |
| id | doaj-art-2347535812264167afcba8ba160cb84c |
| institution | Kabale University |
| issn | 1664-302X |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj-art-2347535812264167afcba8ba160cb84c2025-01-10T11:46:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-12-011510.3389/fmicb.2024.14914851491485A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveumP. E. Contarini0E. Emboule1P. Jean-Louis2T. Woyke3S. V. Date4O. Gros5J-M. Volland6J-M. Volland7J-M. Volland8Institut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Pointe-à-Pitre, FranceInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Pointe-à-Pitre, FranceInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Pointe-à-Pitre, FranceDepartment of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA, United StatesLaboratory for Research in Complex Systems, Menlo Park, CA, United StatesInstitut de Systématique, Evolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, Pointe-à-Pitre, FranceDepartment of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, Santa Barbara, CA, United StatesLaboratory for Research in Complex Systems, Menlo Park, CA, United StatesDepartment of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesSymbiotic interactions drive species evolution, with nutritional symbioses playing vital roles across ecosystems. Chemosynthetic symbioses are globally distributed and ecologically significant, yet the lack of model systems has hindered research progress. The giant ciliate Zoothamnium niveum and its sulfur-oxidizing symbionts represent the only known chemosynthetic symbiosis with a short life span that has been transiently cultivated in the laboratory. While it is experimentally tractable and presents a promising model system, it currently lacks an open-source, simple, and standardized cultivation setup. Following the FABricated Ecosystems (EcoFABs) model, we leveraged 3D printing and polydimethylsiloxane (PDMS) casting to develop simple flow-through cultivation chambers that can be produced and adopted by any laboratory. The streamlined manufacturing process reduces production time by 86% and cuts cost by tenfold compared to the previous system. Benchmarking using previously established optimal growth conditions, the new open-source cultivation system proves stable, efficient, more autonomous, and promotes a more prolific growth of the symbiosis. For the first time, starting from single cells, we successfully cultivated the symbiosis in flow-through chambers for 20 days, spanning multiple generations of colonies that remained symbiotic. They were transferred from chamber to chamber enabling long-term cultivation and eliminating the need for continuous field sampling. The chambers, optimized for live imaging, allowed detailed observation of the synchronized growth between the host and symbiont. Highlighting the benefit of this new system, we here describe a new step in the first hours of development where the host pauses growth, expels a coat, before resuming growth, hinting at a putative symbiont selection mechanism early in the colony life cycle. With this simple, open-source, cultivation setup, Z. niveum holds promises for comparative studies, standardization of research and wide adoption by the symbiosis research community.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491485/fullmutualismcooperationsulphidethiotrophicprotistflow-through |
| spellingShingle | P. E. Contarini E. Emboule P. Jean-Louis T. Woyke S. V. Date O. Gros J-M. Volland J-M. Volland J-M. Volland A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum Frontiers in Microbiology mutualism cooperation sulphide thiotrophic protist flow-through |
| title | A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum |
| title_full | A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum |
| title_fullStr | A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum |
| title_full_unstemmed | A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum |
| title_short | A novel open-source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate Zoothamnium niveum |
| title_sort | novel open source cultivation system helps establish the first full cycle chemosynthetic symbiosis model system involving the giant ciliate zoothamnium niveum |
| topic | mutualism cooperation sulphide thiotrophic protist flow-through |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1491485/full |
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