No Evidence That Nitrogen Limitation Influences the Elemental Composition of Isopod Transcriptomes and Proteomes

• Published in: Molecular biology and evolution 2016-10, Vol.33 (10), p.2605-2620
• Main Authors: Francois, Clémentine M, Duret, Laurent, Simon, Laurent, Mermillod-Blondin, Florian, Malard, Florian, Konecny-Dupré, Lara, Planel, Rémi, Penel, Simon, Douady, Christophe J, Lefébure, Tristan
• Format: Article
• Language: English
• Subjects: Amino Acids - genetics; Amino Acids - metabolism; Animals; Biodiversity and Ecology; Ecosystem; Environmental Sciences; Isopoda - genetics; Isopoda - metabolism; Nitrogen - deficiency; Nitrogen - metabolism; Nucleotides - genetics; Nucleotides - metabolism; Phylogeny; Proteome; Selection, Genetic; Transcriptome
• ISSN: 0737-4038; 1537-1719
• DOI: 10.1093/molbev/msw131

The field of stoichiogenomics aims at understanding the influence of nutrient limitations on the elemental composition of the genome, transcriptome, and proteome. The 20 amino acids and the 4 nt differ in the number of nutrients they contain, such as nitrogen (N). Thus, N limitation shall theoretically select for changes in the composition of proteins or RNAs through preferential use of N-poor amino acids or nucleotides, which will decrease the N-budget of an organism. While these N-saving mechanisms have been evidenced in microorganisms, they remain controversial in multicellular eukaryotes. In this study, we used 13 surface and subterranean isopod species pairs that face strongly contrasted N limitations, either in terms of quantity or quality. We combined in situ nutrient quantification and transcriptome sequencing to test if N limitation selected for N-savings through changes in the expression and composition of the transcriptome and proteome. No evidence of N-savings was found in the total N-budget of transcriptomes or proteomes or in the average protein N-cost. Nevertheless, subterranean species evolving in N-depleted habitats displayed lower N-usage at their third codon positions. To test if this convergent compositional change was driven by natural selection, we developed a method to detect the strand-asymmetric signature that stoichiogenomic selection should leave in the substitution pattern. No such signature was evidenced, indicating that the observed stoichiogenomic-like patterns were attributable to nonadaptive processes. The absence of stoichiogenomic signal despite strong N limitation within a powerful phylogenetic framework casts doubt on the existence of stoichiogenomic mechanisms in metazoans.