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Saturating growth rate against phosphorus concentration explained by macromolecular allocation

The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed, yet the mechanisms behind the relationship remain elusive. Here, we use a mechanistic model of phytoplankton and show that the saturating relationship between growth rate...

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Autores principales: Armin, Gabrielle, Kim, Jongsun, Inomura, Keisuke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654069/
https://www.ncbi.nlm.nih.gov/pubmed/37642424
http://dx.doi.org/10.1128/msystems.00611-23
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author Armin, Gabrielle
Kim, Jongsun
Inomura, Keisuke
author_facet Armin, Gabrielle
Kim, Jongsun
Inomura, Keisuke
author_sort Armin, Gabrielle
collection PubMed
description The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed, yet the mechanisms behind the relationship remain elusive. Here, we use a mechanistic model of phytoplankton and show that the saturating relationship between growth rate and phosphorous concentration can be interpreted by intracellular macromolecular allocation. At low nutrient levels, the diffusive nutrient transport linearly increases with the phosphorous concentration, while the internal phosphorous requirement increases with the growth rate, leading to a non-linear increase in the growth rate with phosphorous. This increased phosphorous requirement is due to the increased allocation to biosynthetic and photosynthetic molecules. The allocation to these molecules reaches a maximum at high-phosphorous concentration, and the growth rate no longer increases despite the rise in phosphorous concentration. The produced growth rate and phosphorous relationships are consistent with the data of phytoplankton across taxa. Our study suggests that the key control of phytoplankton growth is internal, and nutrient uptake is only a single step in the overall process. IMPORTANCE: The Monod equation has been used to represent the relationship between growth rate and the environmental nutrient concentration under the limitation of this respective nutrient. This model often serves as a means to connect microorganisms to their environment, specifically in ecosystem and global models. Here, we use a simple model of a marine microorganism cell to illustrate the model’s ability to capture the same relationship as Monod, while highlighting the additional physiological details our model provides. In this study, we focus on the relationship between growth rate and phosphorus concentration and find that RNA allocation largely contributes to the commonly observed trend. This work emphasizes the potential role our model could play in connecting microorganisms to the surrounding environment while using realistic physiological representations.
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spelling pubmed-106540692023-08-29 Saturating growth rate against phosphorus concentration explained by macromolecular allocation Armin, Gabrielle Kim, Jongsun Inomura, Keisuke mSystems Research Article The saturating relationship between phytoplankton growth rate and environmental nutrient concentration has been widely observed, yet the mechanisms behind the relationship remain elusive. Here, we use a mechanistic model of phytoplankton and show that the saturating relationship between growth rate and phosphorous concentration can be interpreted by intracellular macromolecular allocation. At low nutrient levels, the diffusive nutrient transport linearly increases with the phosphorous concentration, while the internal phosphorous requirement increases with the growth rate, leading to a non-linear increase in the growth rate with phosphorous. This increased phosphorous requirement is due to the increased allocation to biosynthetic and photosynthetic molecules. The allocation to these molecules reaches a maximum at high-phosphorous concentration, and the growth rate no longer increases despite the rise in phosphorous concentration. The produced growth rate and phosphorous relationships are consistent with the data of phytoplankton across taxa. Our study suggests that the key control of phytoplankton growth is internal, and nutrient uptake is only a single step in the overall process. IMPORTANCE: The Monod equation has been used to represent the relationship between growth rate and the environmental nutrient concentration under the limitation of this respective nutrient. This model often serves as a means to connect microorganisms to their environment, specifically in ecosystem and global models. Here, we use a simple model of a marine microorganism cell to illustrate the model’s ability to capture the same relationship as Monod, while highlighting the additional physiological details our model provides. In this study, we focus on the relationship between growth rate and phosphorus concentration and find that RNA allocation largely contributes to the commonly observed trend. This work emphasizes the potential role our model could play in connecting microorganisms to the surrounding environment while using realistic physiological representations. American Society for Microbiology 2023-08-29 /pmc/articles/PMC10654069/ /pubmed/37642424 http://dx.doi.org/10.1128/msystems.00611-23 Text en Copyright © 2023 Armin et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Armin, Gabrielle
Kim, Jongsun
Inomura, Keisuke
Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title_full Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title_fullStr Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title_full_unstemmed Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title_short Saturating growth rate against phosphorus concentration explained by macromolecular allocation
title_sort saturating growth rate against phosphorus concentration explained by macromolecular allocation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10654069/
https://www.ncbi.nlm.nih.gov/pubmed/37642424
http://dx.doi.org/10.1128/msystems.00611-23
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