Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner
Most microorganisms exist in interacting consortia, yet the principles behind consortia assembly, including trading partner structure, still require deciphering, despite being central to understanding, building, and controlling consortia. This study tests a cellular-economy-based hypothesis that pro...
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2025
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| _version_ | 1852015848794882048 |
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| author | Martina Du (22411316) |
| author2 | Jeremy M. Chaćon (22411319) Heejoon Park (22411322) Campbell Putnam (22411325) Tomáš Gedeon (22411328) William R. Harcombe (8259795) Ross P. Carlson (1900651) |
| author2_role | author author author author author author |
| author_facet | Martina Du (22411316) Jeremy M. Chaćon (22411319) Heejoon Park (22411322) Campbell Putnam (22411325) Tomáš Gedeon (22411328) William R. Harcombe (8259795) Ross P. Carlson (1900651) |
| author_role | author |
| dc.creator.none.fl_str_mv | Martina Du (22411316) Jeremy M. Chaćon (22411319) Heejoon Park (22411322) Campbell Putnam (22411325) Tomáš Gedeon (22411328) William R. Harcombe (8259795) Ross P. Carlson (1900651) |
| dc.date.none.fl_str_mv | 2025-10-10T17:50:06Z |
| dc.identifier.none.fl_str_mv | 10.1021/acssynbio.5c00265.s007 |
| dc.relation.none.fl_str_mv | https://figshare.com/articles/dataset/Cellular_Economics_of_Exchanged_Metabolites_Alter_Ratios_of_Microbial_Trading_Partners_in_a_Predictable_Manner/30333548 |
| dc.rights.none.fl_str_mv | CC BY-NC 4.0 info:eu-repo/semantics/openAccess |
| dc.subject.none.fl_str_mv | Biochemistry Genetics Pharmacology Biotechnology Computational Biology Chemical Sciences not elsewhere classified still require deciphering prevented oxidative phosphorylation microbial trading partners equivalent basis provides proposes consortia engaged interpreting natural consortia strain ratios represented predicted strain ratios biological energy density metabolic burden associated equivalent metabolic burden controlling bioprocess consortia quantifying exchanged metabolites atp synthase enzyme 2 </ sub obligate metabolite exchange strain ratios could metabolic burden theory metabolic burden controlling consortia exchanged metabolites metabolite exchange interacting consortia substrate energy obligatory exchange cellular energy study tests predictably shared predictable manner microorganisms exist instead retained fold using flux magnitude |
| dc.title.none.fl_str_mv | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| dc.type.none.fl_str_mv | Dataset info:eu-repo/semantics/publishedVersion dataset |
| description | Most microorganisms exist in interacting consortia, yet the principles behind consortia assembly, including trading partner structure, still require deciphering, despite being central to understanding, building, and controlling consortia. This study tests a cellular-economy-based hypothesis that proposes consortia engaged in obligate metabolite exchange will assemble at ratios where the metabolic burden associated with the exchanges is predictably shared. The metabolic burden was quantified using ATP equivalents, the quantity of high-energy ATP phosphoanhydride bonds that could be produced if the exchanged metabolites were instead retained and catabolized for cellular energy. The hypothesis was tested using Escherichia coli cocultures engineered for obligatory exchange of pyruvate and l-arginine. The burden of metabolite exchange was manipulated by changing the availability of O<sub>2</sub>, which altered the bioavailability of substrate energy, and by deactivating the ATP synthase enzyme, which prevented oxidative phosphorylation. Three synthetic cocultures assembled at predicted strain ratios as a function of perturbations. The strain ratios represented an equivalent metabolic burden between the trading partners even though the exchanged metabolites varied substantially in flux magnitude (300+ fold), molecular weight (174 vs 88 g mol<sup>–1</sup>), enzyme requirements (8 specialized enzymes vs none), and biological energy density (27.5 vs 9 ATP molecule<sup>–1</sup>). The strain ratios could be rationally altered up to 20-fold using O<sub>2</sub> availability and cellular phenotype. The metabolic burden theory was applied to seven additional published cocultures and was found to accurately predict trading partner ratios. Quantifying exchanged metabolites on an ATP-equivalent basis provides a theory for interpreting natural consortia and a toolbox for controlling bioprocess consortia. |
| eu_rights_str_mv | openAccess |
| id | Manara_f9104ef9e85641919f027a94c601079e |
| identifier_str_mv | 10.1021/acssynbio.5c00265.s007 |
| network_acronym_str | Manara |
| network_name_str | ManaraRepo |
| oai_identifier_str | oai:figshare.com:article/30333548 |
| publishDate | 2025 |
| repository.mail.fl_str_mv | |
| repository.name.fl_str_mv | |
| repository_id_str | |
| rights_invalid_str_mv | CC BY-NC 4.0 |
| spelling | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable MannerMartina Du (22411316)Jeremy M. Chaćon (22411319)Heejoon Park (22411322)Campbell Putnam (22411325)Tomáš Gedeon (22411328)William R. Harcombe (8259795)Ross P. Carlson (1900651)BiochemistryGeneticsPharmacologyBiotechnologyComputational BiologyChemical Sciences not elsewhere classifiedstill require decipheringprevented oxidative phosphorylationmicrobial trading partnersequivalent basis providesproposes consortia engagedinterpreting natural consortiastrain ratios representedpredicted strain ratiosbiological energy densitymetabolic burden associatedequivalent metabolic burdencontrolling bioprocess consortiaquantifying exchanged metabolitesatp synthase enzyme2 </ subobligate metabolite exchangestrain ratios couldmetabolic burden theorymetabolic burdencontrolling consortiaexchanged metabolitesmetabolite exchangeinteracting consortiasubstrate energyobligatory exchangecellular energystudy testspredictably sharedpredictable mannermicroorganisms existinstead retainedfold usingflux magnitudeMost microorganisms exist in interacting consortia, yet the principles behind consortia assembly, including trading partner structure, still require deciphering, despite being central to understanding, building, and controlling consortia. This study tests a cellular-economy-based hypothesis that proposes consortia engaged in obligate metabolite exchange will assemble at ratios where the metabolic burden associated with the exchanges is predictably shared. The metabolic burden was quantified using ATP equivalents, the quantity of high-energy ATP phosphoanhydride bonds that could be produced if the exchanged metabolites were instead retained and catabolized for cellular energy. The hypothesis was tested using Escherichia coli cocultures engineered for obligatory exchange of pyruvate and l-arginine. The burden of metabolite exchange was manipulated by changing the availability of O<sub>2</sub>, which altered the bioavailability of substrate energy, and by deactivating the ATP synthase enzyme, which prevented oxidative phosphorylation. Three synthetic cocultures assembled at predicted strain ratios as a function of perturbations. The strain ratios represented an equivalent metabolic burden between the trading partners even though the exchanged metabolites varied substantially in flux magnitude (300+ fold), molecular weight (174 vs 88 g mol<sup>–1</sup>), enzyme requirements (8 specialized enzymes vs none), and biological energy density (27.5 vs 9 ATP molecule<sup>–1</sup>). The strain ratios could be rationally altered up to 20-fold using O<sub>2</sub> availability and cellular phenotype. The metabolic burden theory was applied to seven additional published cocultures and was found to accurately predict trading partner ratios. Quantifying exchanged metabolites on an ATP-equivalent basis provides a theory for interpreting natural consortia and a toolbox for controlling bioprocess consortia.2025-10-10T17:50:06ZDatasetinfo:eu-repo/semantics/publishedVersiondataset10.1021/acssynbio.5c00265.s007https://figshare.com/articles/dataset/Cellular_Economics_of_Exchanged_Metabolites_Alter_Ratios_of_Microbial_Trading_Partners_in_a_Predictable_Manner/30333548CC BY-NC 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/303335482025-10-10T17:50:06Z |
| spellingShingle | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner Martina Du (22411316) Biochemistry Genetics Pharmacology Biotechnology Computational Biology Chemical Sciences not elsewhere classified still require deciphering prevented oxidative phosphorylation microbial trading partners equivalent basis provides proposes consortia engaged interpreting natural consortia strain ratios represented predicted strain ratios biological energy density metabolic burden associated equivalent metabolic burden controlling bioprocess consortia quantifying exchanged metabolites atp synthase enzyme 2 </ sub obligate metabolite exchange strain ratios could metabolic burden theory metabolic burden controlling consortia exchanged metabolites metabolite exchange interacting consortia substrate energy obligatory exchange cellular energy study tests predictably shared predictable manner microorganisms exist instead retained fold using flux magnitude |
| status_str | publishedVersion |
| title | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| title_full | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| title_fullStr | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| title_full_unstemmed | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| title_short | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| title_sort | Cellular Economics of Exchanged Metabolites Alter Ratios of Microbial Trading Partners in a Predictable Manner |
| topic | Biochemistry Genetics Pharmacology Biotechnology Computational Biology Chemical Sciences not elsewhere classified still require deciphering prevented oxidative phosphorylation microbial trading partners equivalent basis provides proposes consortia engaged interpreting natural consortia strain ratios represented predicted strain ratios biological energy density metabolic burden associated equivalent metabolic burden controlling bioprocess consortia quantifying exchanged metabolites atp synthase enzyme 2 </ sub obligate metabolite exchange strain ratios could metabolic burden theory metabolic burden controlling consortia exchanged metabolites metabolite exchange interacting consortia substrate energy obligatory exchange cellular energy study tests predictably shared predictable manner microorganisms exist instead retained fold using flux magnitude |