Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways.
During photoheterotrophic growth on organic substrates, purple nonsulfur photosynthetic bacteria like Rhodospirillum rubrum can acquire electrons by multiple means, including oxidation of organic substrates, oxidation of inorganic electron donors (e.g., H2), and by reverse electron flow from the pho...
Saved in:
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2025-06-01
|
| Series: | PLoS Computational Biology |
| Online Access: | https://doi.org/10.1371/journal.pcbi.1013015 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850220689540251648 |
|---|---|
| author | William R Cannon Ethan King Katherine A Huening Justin A North |
| author_facet | William R Cannon Ethan King Katherine A Huening Justin A North |
| author_sort | William R Cannon |
| collection | DOAJ |
| description | During photoheterotrophic growth on organic substrates, purple nonsulfur photosynthetic bacteria like Rhodospirillum rubrum can acquire electrons by multiple means, including oxidation of organic substrates, oxidation of inorganic electron donors (e.g., H2), and by reverse electron flow from the photosynthetic electron transport chain. These electrons are stored as reduced electron-carrying cofactors (e.g., NAD(P)H and ferredoxin). The overall ratio of oxidized to reduced cofactors (e.g., NAD(P)+:NAD(P)H), or 'redox poise', is difficult to understand or predict, as are the cellular processes for dissipating these reducing equivalents. Using physics-based models that capture mass action kinetics consistent with the thermodynamics of reactions and pathways, a range of redox conditions for heterophototrophic growth are evaluated, from conditions in which the NADP+/NADPH levels approach thermodynamic equilibrium to conditions in which the NADP+/NADPH ratio is far above the typical physiological values. Modeling predictions together with experimental measurements indicate that the redox poise of the cell results in large-scale changes in the activity of biosynthetic pathways and, thus, changes in cell macromolecule levels (DNA, RNA, proteins, and fatty acids). Furthermore, modeling predictions indicate that during phototrophic growth, reverse electron flow from the quinone pool is a minor contributor to the production of reduced cofactors (e.g., NAD(P)H) compared to other oxidative processes (H2 and carbon substrate oxidation). Instead, the quinone pool primarily operates to aid ATP production. The high level of ATP, in turn, drives reduction processes even when NADPH levels are relatively low compared to NADP+ by coupling ATP hydrolysis to the reductive processes. The model, in agreement with experimental measurements of macromolecule ratios of cells growing on different carbon substrates, indicates that the dynamics of nucleotide versus lipid and protein production is likely a significant mechanism of balancing oxidation and reduction in the cell. |
| format | Article |
| id | doaj-art-b803063bb5f74e6abc1ec25c5fd59818 |
| institution | OA Journals |
| issn | 1553-734X 1553-7358 |
| language | English |
| publishDate | 2025-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj-art-b803063bb5f74e6abc1ec25c5fd598182025-08-20T02:06:58ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582025-06-01216e101301510.1371/journal.pcbi.1013015Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways.William R CannonEthan KingKatherine A HueningJustin A NorthDuring photoheterotrophic growth on organic substrates, purple nonsulfur photosynthetic bacteria like Rhodospirillum rubrum can acquire electrons by multiple means, including oxidation of organic substrates, oxidation of inorganic electron donors (e.g., H2), and by reverse electron flow from the photosynthetic electron transport chain. These electrons are stored as reduced electron-carrying cofactors (e.g., NAD(P)H and ferredoxin). The overall ratio of oxidized to reduced cofactors (e.g., NAD(P)+:NAD(P)H), or 'redox poise', is difficult to understand or predict, as are the cellular processes for dissipating these reducing equivalents. Using physics-based models that capture mass action kinetics consistent with the thermodynamics of reactions and pathways, a range of redox conditions for heterophototrophic growth are evaluated, from conditions in which the NADP+/NADPH levels approach thermodynamic equilibrium to conditions in which the NADP+/NADPH ratio is far above the typical physiological values. Modeling predictions together with experimental measurements indicate that the redox poise of the cell results in large-scale changes in the activity of biosynthetic pathways and, thus, changes in cell macromolecule levels (DNA, RNA, proteins, and fatty acids). Furthermore, modeling predictions indicate that during phototrophic growth, reverse electron flow from the quinone pool is a minor contributor to the production of reduced cofactors (e.g., NAD(P)H) compared to other oxidative processes (H2 and carbon substrate oxidation). Instead, the quinone pool primarily operates to aid ATP production. The high level of ATP, in turn, drives reduction processes even when NADPH levels are relatively low compared to NADP+ by coupling ATP hydrolysis to the reductive processes. The model, in agreement with experimental measurements of macromolecule ratios of cells growing on different carbon substrates, indicates that the dynamics of nucleotide versus lipid and protein production is likely a significant mechanism of balancing oxidation and reduction in the cell.https://doi.org/10.1371/journal.pcbi.1013015 |
| spellingShingle | William R Cannon Ethan King Katherine A Huening Justin A North Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. PLoS Computational Biology |
| title | Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. |
| title_full | Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. |
| title_fullStr | Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. |
| title_full_unstemmed | Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. |
| title_short | Redox poise in R. rubrum phototrophic growth drives large-scale changes in macromolecular pathways. |
| title_sort | redox poise in r rubrum phototrophic growth drives large scale changes in macromolecular pathways |
| url | https://doi.org/10.1371/journal.pcbi.1013015 |
| work_keys_str_mv | AT williamrcannon redoxpoiseinrrubrumphototrophicgrowthdriveslargescalechangesinmacromolecularpathways AT ethanking redoxpoiseinrrubrumphototrophicgrowthdriveslargescalechangesinmacromolecularpathways AT katherineahuening redoxpoiseinrrubrumphototrophicgrowthdriveslargescalechangesinmacromolecularpathways AT justinanorth redoxpoiseinrrubrumphototrophicgrowthdriveslargescalechangesinmacromolecularpathways |