Fundamental connections among organism C: N:P stoichiometry, macromolecular composition, and growth

Tobias Vrede, Dean R. Dobberfuhl, S. A L M Kooijman, James Elser

Research output: Contribution to journalArticle

151 Citations (Scopus)

Abstract

Whereas it is acknowledged that the C:N:P stoichiometry of consumers and their resources affects both the structure and the function of food webs, and eventually influences broad-scale processes such as global carbon cycles, the mechanistic basis for the variation in stoichiometry has not yet been fully explored. Empirical evidence shows that the specific growth rate is positively related to RNA concentration both between and within taxa in both unicellular and multicellular organisms. Since RNA is rich in P and constitutes a substantial part of the total P in organisms, a high growth rate is also connected with a high P content. We argue that the reason for this pattern is that the growth of all biota is closely linked with their protein synthesis rate, and thus with the concentration of ribosomal RNA. Dynamic energy budget theory supports the positive relationship between RNA and specific growth rate in microorganisms, whereas the predictions concerning multicellulars only partially agrees with the observed pattern. In a simple model of consumer growth, we explore the consequences of various allocation patterns of RNA, protein, carbohydrates/lipids, and other biochemical constituents on organism potential growth rate and C:N:P stoichiometry. According to the model the percentage of N and especially percentage of P per dry mass increases with increasing specific growth rate. Furthermore, the model suggests that macromolecule allocation patterns and thus N:P stoichiometry are allowed to differ substantially at low growth rates whereas the stoichiometry at high growth rates is much more constricted at low N:P. The model fits empirical data reasonably well, but it is also acknowledged that complex life cycles and associated physiological constraints may result in other patterns. We also use a similar approach of modeling organism growth from basic biochemical principles to illustrate fundamental connections among biochemical allocation and C:N stoichiometry in autotroph production, which is based on allocation patterns between carbohydrates and rubisco. Similar to the RNA-protein model, macromolecular composition and C:N ratios are more constrained at high than at low growth rates. The models and the empirical data together suggest that organism growth is tightly linked with the organisms' biochemical and elemental composition. The stoichiometry of growth impinges on nutrient cycles and carbon fluxes at the ecosystem level. Thus, focus on the biological basis of organism C:N:P stoichiometry can mechanistically connect growth strategy and biochemical and cellular mechanisms of biota to major ecological consequences.

Original languageEnglish (US)
Pages (from-to)1217-1229
Number of pages13
JournalEcology
Volume85
Issue number5
StatePublished - May 2004

Fingerprint

stoichiometry
RNA
organisms
specific growth rate
protein
biota
carbohydrate
carbohydrates
organism
carbon flux
energy budget
carbon cycle
autotrophs
ribulose-bisphosphate carboxylase
food web
carbon nitrogen ratio
biogeochemical cycles
food webs
life cycle
microorganism

Keywords

  • Autotroph production
  • C:N:P stoichiometry
  • Consumer growth rate
  • Dynamic energy budget theory
  • Macromolecular allocation patterns
  • Protein allocation
  • Ribosomal RNA
  • Rubisco

ASJC Scopus subject areas

  • Ecology

Cite this

Vrede, T., Dobberfuhl, D. R., Kooijman, S. A. L. M., & Elser, J. (2004). Fundamental connections among organism C: N:P stoichiometry, macromolecular composition, and growth. Ecology, 85(5), 1217-1229.

Fundamental connections among organism C : N:P stoichiometry, macromolecular composition, and growth. / Vrede, Tobias; Dobberfuhl, Dean R.; Kooijman, S. A L M; Elser, James.

In: Ecology, Vol. 85, No. 5, 05.2004, p. 1217-1229.

Research output: Contribution to journalArticle

Vrede, T, Dobberfuhl, DR, Kooijman, SALM & Elser, J 2004, 'Fundamental connections among organism C: N:P stoichiometry, macromolecular composition, and growth', Ecology, vol. 85, no. 5, pp. 1217-1229.
Vrede, Tobias ; Dobberfuhl, Dean R. ; Kooijman, S. A L M ; Elser, James. / Fundamental connections among organism C : N:P stoichiometry, macromolecular composition, and growth. In: Ecology. 2004 ; Vol. 85, No. 5. pp. 1217-1229.
@article{f496c3e5548642d08666e141fbb49876,
title = "Fundamental connections among organism C: N:P stoichiometry, macromolecular composition, and growth",
abstract = "Whereas it is acknowledged that the C:N:P stoichiometry of consumers and their resources affects both the structure and the function of food webs, and eventually influences broad-scale processes such as global carbon cycles, the mechanistic basis for the variation in stoichiometry has not yet been fully explored. Empirical evidence shows that the specific growth rate is positively related to RNA concentration both between and within taxa in both unicellular and multicellular organisms. Since RNA is rich in P and constitutes a substantial part of the total P in organisms, a high growth rate is also connected with a high P content. We argue that the reason for this pattern is that the growth of all biota is closely linked with their protein synthesis rate, and thus with the concentration of ribosomal RNA. Dynamic energy budget theory supports the positive relationship between RNA and specific growth rate in microorganisms, whereas the predictions concerning multicellulars only partially agrees with the observed pattern. In a simple model of consumer growth, we explore the consequences of various allocation patterns of RNA, protein, carbohydrates/lipids, and other biochemical constituents on organism potential growth rate and C:N:P stoichiometry. According to the model the percentage of N and especially percentage of P per dry mass increases with increasing specific growth rate. Furthermore, the model suggests that macromolecule allocation patterns and thus N:P stoichiometry are allowed to differ substantially at low growth rates whereas the stoichiometry at high growth rates is much more constricted at low N:P. The model fits empirical data reasonably well, but it is also acknowledged that complex life cycles and associated physiological constraints may result in other patterns. We also use a similar approach of modeling organism growth from basic biochemical principles to illustrate fundamental connections among biochemical allocation and C:N stoichiometry in autotroph production, which is based on allocation patterns between carbohydrates and rubisco. Similar to the RNA-protein model, macromolecular composition and C:N ratios are more constrained at high than at low growth rates. The models and the empirical data together suggest that organism growth is tightly linked with the organisms' biochemical and elemental composition. The stoichiometry of growth impinges on nutrient cycles and carbon fluxes at the ecosystem level. Thus, focus on the biological basis of organism C:N:P stoichiometry can mechanistically connect growth strategy and biochemical and cellular mechanisms of biota to major ecological consequences.",
keywords = "Autotroph production, C:N:P stoichiometry, Consumer growth rate, Dynamic energy budget theory, Macromolecular allocation patterns, Protein allocation, Ribosomal RNA, Rubisco",
author = "Tobias Vrede and Dobberfuhl, {Dean R.} and Kooijman, {S. A L M} and James Elser",
year = "2004",
month = "5",
language = "English (US)",
volume = "85",
pages = "1217--1229",
journal = "Ecology",
issn = "0012-9658",
publisher = "Ecological Society of America",
number = "5",

}

TY - JOUR

T1 - Fundamental connections among organism C

T2 - N:P stoichiometry, macromolecular composition, and growth

AU - Vrede, Tobias

AU - Dobberfuhl, Dean R.

AU - Kooijman, S. A L M

AU - Elser, James

PY - 2004/5

Y1 - 2004/5

N2 - Whereas it is acknowledged that the C:N:P stoichiometry of consumers and their resources affects both the structure and the function of food webs, and eventually influences broad-scale processes such as global carbon cycles, the mechanistic basis for the variation in stoichiometry has not yet been fully explored. Empirical evidence shows that the specific growth rate is positively related to RNA concentration both between and within taxa in both unicellular and multicellular organisms. Since RNA is rich in P and constitutes a substantial part of the total P in organisms, a high growth rate is also connected with a high P content. We argue that the reason for this pattern is that the growth of all biota is closely linked with their protein synthesis rate, and thus with the concentration of ribosomal RNA. Dynamic energy budget theory supports the positive relationship between RNA and specific growth rate in microorganisms, whereas the predictions concerning multicellulars only partially agrees with the observed pattern. In a simple model of consumer growth, we explore the consequences of various allocation patterns of RNA, protein, carbohydrates/lipids, and other biochemical constituents on organism potential growth rate and C:N:P stoichiometry. According to the model the percentage of N and especially percentage of P per dry mass increases with increasing specific growth rate. Furthermore, the model suggests that macromolecule allocation patterns and thus N:P stoichiometry are allowed to differ substantially at low growth rates whereas the stoichiometry at high growth rates is much more constricted at low N:P. The model fits empirical data reasonably well, but it is also acknowledged that complex life cycles and associated physiological constraints may result in other patterns. We also use a similar approach of modeling organism growth from basic biochemical principles to illustrate fundamental connections among biochemical allocation and C:N stoichiometry in autotroph production, which is based on allocation patterns between carbohydrates and rubisco. Similar to the RNA-protein model, macromolecular composition and C:N ratios are more constrained at high than at low growth rates. The models and the empirical data together suggest that organism growth is tightly linked with the organisms' biochemical and elemental composition. The stoichiometry of growth impinges on nutrient cycles and carbon fluxes at the ecosystem level. Thus, focus on the biological basis of organism C:N:P stoichiometry can mechanistically connect growth strategy and biochemical and cellular mechanisms of biota to major ecological consequences.

AB - Whereas it is acknowledged that the C:N:P stoichiometry of consumers and their resources affects both the structure and the function of food webs, and eventually influences broad-scale processes such as global carbon cycles, the mechanistic basis for the variation in stoichiometry has not yet been fully explored. Empirical evidence shows that the specific growth rate is positively related to RNA concentration both between and within taxa in both unicellular and multicellular organisms. Since RNA is rich in P and constitutes a substantial part of the total P in organisms, a high growth rate is also connected with a high P content. We argue that the reason for this pattern is that the growth of all biota is closely linked with their protein synthesis rate, and thus with the concentration of ribosomal RNA. Dynamic energy budget theory supports the positive relationship between RNA and specific growth rate in microorganisms, whereas the predictions concerning multicellulars only partially agrees with the observed pattern. In a simple model of consumer growth, we explore the consequences of various allocation patterns of RNA, protein, carbohydrates/lipids, and other biochemical constituents on organism potential growth rate and C:N:P stoichiometry. According to the model the percentage of N and especially percentage of P per dry mass increases with increasing specific growth rate. Furthermore, the model suggests that macromolecule allocation patterns and thus N:P stoichiometry are allowed to differ substantially at low growth rates whereas the stoichiometry at high growth rates is much more constricted at low N:P. The model fits empirical data reasonably well, but it is also acknowledged that complex life cycles and associated physiological constraints may result in other patterns. We also use a similar approach of modeling organism growth from basic biochemical principles to illustrate fundamental connections among biochemical allocation and C:N stoichiometry in autotroph production, which is based on allocation patterns between carbohydrates and rubisco. Similar to the RNA-protein model, macromolecular composition and C:N ratios are more constrained at high than at low growth rates. The models and the empirical data together suggest that organism growth is tightly linked with the organisms' biochemical and elemental composition. The stoichiometry of growth impinges on nutrient cycles and carbon fluxes at the ecosystem level. Thus, focus on the biological basis of organism C:N:P stoichiometry can mechanistically connect growth strategy and biochemical and cellular mechanisms of biota to major ecological consequences.

KW - Autotroph production

KW - C:N:P stoichiometry

KW - Consumer growth rate

KW - Dynamic energy budget theory

KW - Macromolecular allocation patterns

KW - Protein allocation

KW - Ribosomal RNA

KW - Rubisco

UR - http://www.scopus.com/inward/record.url?scp=4444280827&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=4444280827&partnerID=8YFLogxK

M3 - Article

AN - SCOPUS:4444280827

VL - 85

SP - 1217

EP - 1229

JO - Ecology

JF - Ecology

SN - 0012-9658

IS - 5

ER -