High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803
ABSTRACTCyanobacteria fix carbon dioxide and release carbon-containing compounds into the wider ecosystem, yet they are sensitive to small metabolites that may impact their growth and physiology. Several cyanobacteria can grow mixotrophically, but we currently lack a molecular understanding of how s...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2024-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00227-24 |
| _version_ | 1797205258604118016 |
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| author | Vilhelmiina Haavisto Zachary Landry Sammy Pontrelli |
| author_facet | Vilhelmiina Haavisto Zachary Landry Sammy Pontrelli |
| author_sort | Vilhelmiina Haavisto |
| collection | DOAJ |
| description | ABSTRACTCyanobacteria fix carbon dioxide and release carbon-containing compounds into the wider ecosystem, yet they are sensitive to small metabolites that may impact their growth and physiology. Several cyanobacteria can grow mixotrophically, but we currently lack a molecular understanding of how specific nutrients may alter the compounds they release, limiting our knowledge of how environmental factors might impact primary producers and the ecosystems they support. In this study, we develop a high-throughput phytoplankton culturing platform and identify how the model cyanobacterium Synechocystis sp. PCC 6803 responds to nutrient supplementation. We assess growth responses to 32 nutrients at two concentrations, identifying 15 that are utilized mixotrophically. Seven nutrient sources significantly enhance growth, while 19 elicit negative growth responses at one or both concentrations. High-throughput exometabolomics indicates that oxidative stress limits Synechocystis’ growth but may be alleviated by antioxidant metabolites. Furthermore, glucose and valine induce strong changes in metabolite exudation in a possible effort to correct pathway imbalances or maintain intracellular elemental ratios. This study sheds light on the flexibility and limits of cyanobacterial physiology and metabolism, as well as how primary production and trophic food webs may be modulated by exogenous nutrients.IMPORTANCECyanobacteria capture and release carbon compounds to fuel microbial food webs, yet we lack a comprehensive understanding of how external nutrients modify their behavior and what they produce. We developed a high throughput culturing platform to evaluate how the model cyanobacterium Synechocystis sp. PCC 6803 responds to a broad panel of externally supplied nutrients. We found that growth may be enhanced by metabolites that protect against oxidative stress, and growth and exudate profiles are altered by metabolites that interfere with central carbon metabolism and elemental ratios. This work contributes a holistic perspective of the versatile response of Synechocystis to externally supplied nutrients, which may alter carbon flux into the wider ecosystem. |
| first_indexed | 2024-04-24T08:48:16Z |
| format | Article |
| id | doaj.art-f3e3821f25f24daba9129108895898ac |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-24T08:48:16Z |
| publishDate | 2024-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-f3e3821f25f24daba9129108895898ac2024-04-16T13:00:55ZengAmerican Society for MicrobiologymSystems2379-50772024-04-019410.1128/msystems.00227-24High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803Vilhelmiina Haavisto0Zachary Landry1Sammy Pontrelli2Institute of Molecular Systems Biology, Department of Biology, ETH Zürich, Zürich, SwitzerlandDepartment of Civil, Environmental and Geomatic Engineering, Institute of Environmental Engineering, ETH Zürich, Zürich, SwitzerlandInstitute of Molecular Systems Biology, Department of Biology, ETH Zürich, Zürich, SwitzerlandABSTRACTCyanobacteria fix carbon dioxide and release carbon-containing compounds into the wider ecosystem, yet they are sensitive to small metabolites that may impact their growth and physiology. Several cyanobacteria can grow mixotrophically, but we currently lack a molecular understanding of how specific nutrients may alter the compounds they release, limiting our knowledge of how environmental factors might impact primary producers and the ecosystems they support. In this study, we develop a high-throughput phytoplankton culturing platform and identify how the model cyanobacterium Synechocystis sp. PCC 6803 responds to nutrient supplementation. We assess growth responses to 32 nutrients at two concentrations, identifying 15 that are utilized mixotrophically. Seven nutrient sources significantly enhance growth, while 19 elicit negative growth responses at one or both concentrations. High-throughput exometabolomics indicates that oxidative stress limits Synechocystis’ growth but may be alleviated by antioxidant metabolites. Furthermore, glucose and valine induce strong changes in metabolite exudation in a possible effort to correct pathway imbalances or maintain intracellular elemental ratios. This study sheds light on the flexibility and limits of cyanobacterial physiology and metabolism, as well as how primary production and trophic food webs may be modulated by exogenous nutrients.IMPORTANCECyanobacteria capture and release carbon compounds to fuel microbial food webs, yet we lack a comprehensive understanding of how external nutrients modify their behavior and what they produce. We developed a high throughput culturing platform to evaluate how the model cyanobacterium Synechocystis sp. PCC 6803 responds to a broad panel of externally supplied nutrients. We found that growth may be enhanced by metabolites that protect against oxidative stress, and growth and exudate profiles are altered by metabolites that interfere with central carbon metabolism and elemental ratios. This work contributes a holistic perspective of the versatile response of Synechocystis to externally supplied nutrients, which may alter carbon flux into the wider ecosystem.https://journals.asm.org/doi/10.1128/msystems.00227-24mixotrophySynechocystismetabolomicsenvironmental microbiologymetabolismexometabolomics |
| spellingShingle | Vilhelmiina Haavisto Zachary Landry Sammy Pontrelli High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 mSystems mixotrophy Synechocystis metabolomics environmental microbiology metabolism exometabolomics |
| title | High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 |
| title_full | High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 |
| title_fullStr | High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 |
| title_full_unstemmed | High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 |
| title_short | High-throughput profiling of metabolic responses to exogenous nutrients in Synechocystis sp. PCC 6803 |
| title_sort | high throughput profiling of metabolic responses to exogenous nutrients in synechocystis sp pcc 6803 |
| topic | mixotrophy Synechocystis metabolomics environmental microbiology metabolism exometabolomics |
| url | https://journals.asm.org/doi/10.1128/msystems.00227-24 |
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