Signatures of nitrogen limitation in the elemental composition of the proteins involved in the metabolic apparatus

Claudia Acquisti, Sudhir Kumar, James Elser

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

Nitrogen (N) is a fundamental component of nucleotides and amino acids and is often a limiting nutrient in natural ecosystems. Thus, study of the N content of biomolecules may establish important connections between ecology and genomics. However, while significant differences in the elemental composition of whole organisms are well documented, how the flux of nutrients in the cell has shaped the evolution of different cellular processes remains poorly understood. By examining the elemental composition of major functional classes of proteins in four multicellular eukaryotic model organisms, we find that the catabolic machinery shows substantially lower N content than the anabolic machinery and the rest of the proteome. This pattern suggests that ecological selection for N conservation specifically targets cellular components that are highly expressed in response to nutrient limitation. We propose that the RNA component of the anabolic machineries is the mechanistic force driving the elemental imbalance we found, and that RNA functions as an intracellular nutrient reservoir that is degraded and recycled during starvation periods. A comparison of the elemental composition of the anabolic and catabolic machineries in species that have experienced different levels of N limitation in their evolutionary history (animals versus plants) suggests that selection for N conservation has preferentially targeted the catabolic machineries of plants, resulting in a lower N content of the proteins involved in their catabolic processes. These findings link the composition of major cellular components to the environmental factors that trigger the activation of those components, suggesting that resource availability has constrained the atomic composition and the molecular architecture of the biotic processes that enable cells to respond to reduced nutrient availability.

Original languageEnglish (US)
Pages (from-to)2605-2610
Number of pages6
JournalProceedings of the Royal Society B: Biological Sciences
Volume276
Issue number1667
DOIs
StatePublished - Jul 22 2009

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Nutrients
Nitrogen
Food
machinery
protein
RNA
nutrient
nitrogen
nutrients
Chemical analysis
Proteins
proteins
nutrient limitation
Machinery
resource availability
Conservation
nutrient availability
starvation
Availability
organisms

Keywords

  • Biological stoichiometry
  • Cellular components
  • Elemental composition
  • Metabolic apparatus
  • Molecular evolution
  • Nutrient limitation

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Environmental Science(all)
  • Immunology and Microbiology(all)
  • Medicine(all)

Cite this

Signatures of nitrogen limitation in the elemental composition of the proteins involved in the metabolic apparatus. / Acquisti, Claudia; Kumar, Sudhir; Elser, James.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 276, No. 1667, 22.07.2009, p. 2605-2610.

Research output: Contribution to journalArticle

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