Revisiting the growth rate hypothesis: Towards a holistic stoichiometric understanding of growth

Jana Isanta-Navarro; Clay Prater; Logan M. Peoples; Irakli Loladze; Tin Phan; Punidan D. Jeyasingh; Matthew J. Church; Yang Kuang; James J. Elser

doi:10.1111/ele.14096

Revisiting the growth rate hypothesis: Towards a holistic stoichiometric understanding of growth

Jana Isanta-Navarro, Clay Prater, Logan M. Peoples, Irakli Loladze, Tin Phan, Punidan D. Jeyasingh, Matthew J. Church, Yang Kuang, James J. Elser

Flathead Lake Biological Station

Research output: Contribution to journal › Article › peer-review

48 Scopus citations

Abstract

The growth rate hypothesis (GRH) posits that variation in organismal stoichiometry (C:P and N:P ratios) is driven by growth-dependent allocation of P to ribosomal RNA. The GRH has found broad but not uniform support in studies across diverse biota and habitats. We synthesise information on how and why the tripartite growth-RNA-P relationship predicted by the GRH may be uncoupled and outline paths for both theoretical and empirical work needed to broaden the working domain of the GRH. We found strong support for growth to RNA (r² = 0.59) and RNA-P to P (r² = 0.63) relationships across taxa, but growth to P relationships were relatively weaker (r² = 0.09). Together, the GRH was supported in ~50% of studies. Mechanisms behind GRH uncoupling were diverse but could generally be attributed to physiological (P accumulation in non-RNA pools, inactive ribosomes, translation elongation rates and protein turnover rates), ecological (limitation by resources other than P), and evolutionary (adaptation to different nutrient supply regimes) causes. These factors should be accounted for in empirical tests of the GRH and formalised mathematically to facilitate a predictive understanding of growth.

Original language	English
Pages (from-to)	2324-2339
Number of pages	16
Journal	Ecology Letters
Volume	25
Issue number	10
DOIs	https://doi.org/10.1111/ele.14096
State	Published - Oct 2022

Funding

We thank Paul Frost and two anonymous reviewers for valuable feedback that improved the quality of this paper. This study largely benefited from the numerous data sets that were provided by colleagues around the world. We would like to thank all researchers who responded to our inquiry and shared their data. This work was supported by the US National Science Foundation Rules of Life programme (DEB‐1930816 to JJE and MJC, DEB‐1930736 to PDJ and DEB ‐1930728 to YK and IL). YK is also partially supported by NIH grant 5R01GM131405‐02.

Funder number
DEB‐1930816, DEB ‐1930728, DEB‐1930736
R01GM131405

Keywords

RNA
carbon
ecological stoichiometry
growth rate hypothesis
nitrogen
phosphorus
protein

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10.1111/ele.14096

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title = "Revisiting the growth rate hypothesis: Towards a holistic stoichiometric understanding of growth",

abstract = "The growth rate hypothesis (GRH) posits that variation in organismal stoichiometry (C:P and N:P ratios) is driven by growth-dependent allocation of P to ribosomal RNA. The GRH has found broad but not uniform support in studies across diverse biota and habitats. We synthesise information on how and why the tripartite growth-RNA-P relationship predicted by the GRH may be uncoupled and outline paths for both theoretical and empirical work needed to broaden the working domain of the GRH. We found strong support for growth to RNA (r2 = 0.59) and RNA-P to P (r2 = 0.63) relationships across taxa, but growth to P relationships were relatively weaker (r2 = 0.09). Together, the GRH was supported in \textasciitilde{}50\% of studies. Mechanisms behind GRH uncoupling were diverse but could generally be attributed to physiological (P accumulation in non-RNA pools, inactive ribosomes, translation elongation rates and protein turnover rates), ecological (limitation by resources other than P), and evolutionary (adaptation to different nutrient supply regimes) causes. These factors should be accounted for in empirical tests of the GRH and formalised mathematically to facilitate a predictive understanding of growth.",

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author = "Jana Isanta-Navarro and Clay Prater and Peoples, \{Logan M.\} and Irakli Loladze and Tin Phan and Jeyasingh, \{Punidan D.\} and Church, \{Matthew J.\} and Yang Kuang and Elser, \{James J.\}",

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year = "2022",

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AU - Isanta-Navarro, Jana

AU - Prater, Clay

AU - Peoples, Logan M.

AU - Loladze, Irakli

AU - Phan, Tin

AU - Jeyasingh, Punidan D.

AU - Church, Matthew J.

AU - Kuang, Yang

AU - Elser, James J.

PY - 2022/10

Y1 - 2022/10

N2 - The growth rate hypothesis (GRH) posits that variation in organismal stoichiometry (C:P and N:P ratios) is driven by growth-dependent allocation of P to ribosomal RNA. The GRH has found broad but not uniform support in studies across diverse biota and habitats. We synthesise information on how and why the tripartite growth-RNA-P relationship predicted by the GRH may be uncoupled and outline paths for both theoretical and empirical work needed to broaden the working domain of the GRH. We found strong support for growth to RNA (r2 = 0.59) and RNA-P to P (r2 = 0.63) relationships across taxa, but growth to P relationships were relatively weaker (r2 = 0.09). Together, the GRH was supported in ~50% of studies. Mechanisms behind GRH uncoupling were diverse but could generally be attributed to physiological (P accumulation in non-RNA pools, inactive ribosomes, translation elongation rates and protein turnover rates), ecological (limitation by resources other than P), and evolutionary (adaptation to different nutrient supply regimes) causes. These factors should be accounted for in empirical tests of the GRH and formalised mathematically to facilitate a predictive understanding of growth.

AB - The growth rate hypothesis (GRH) posits that variation in organismal stoichiometry (C:P and N:P ratios) is driven by growth-dependent allocation of P to ribosomal RNA. The GRH has found broad but not uniform support in studies across diverse biota and habitats. We synthesise information on how and why the tripartite growth-RNA-P relationship predicted by the GRH may be uncoupled and outline paths for both theoretical and empirical work needed to broaden the working domain of the GRH. We found strong support for growth to RNA (r2 = 0.59) and RNA-P to P (r2 = 0.63) relationships across taxa, but growth to P relationships were relatively weaker (r2 = 0.09). Together, the GRH was supported in ~50% of studies. Mechanisms behind GRH uncoupling were diverse but could generally be attributed to physiological (P accumulation in non-RNA pools, inactive ribosomes, translation elongation rates and protein turnover rates), ecological (limitation by resources other than P), and evolutionary (adaptation to different nutrient supply regimes) causes. These factors should be accounted for in empirical tests of the GRH and formalised mathematically to facilitate a predictive understanding of growth.

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KW - growth rate hypothesis

KW - nitrogen

KW - phosphorus

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Revisiting the growth rate hypothesis: Towards a holistic stoichiometric understanding of growth

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