Evolutionary systems biology of amino acid biosynthetic cost in yeast.

Every protein has a biosynthetic cost to the cell based on the synthesis of its constituent amino acids. In order to optimise growth and reproduction, natural selection is expected, where possible, to favour the use of proteins whose constituents are cheaper to produce, as reduced biosynthetic cost...

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Autores principales:	Michael D Barton, Daniela Delneri, Stephen G Oliver, Magnus Rattray, Casey M Bergman
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2010
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/12202ad9fd7b41cfb56b0f6a1e8ae748
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spelling	oai:doaj.org-article:12202ad9fd7b41cfb56b0f6a1e8ae7482021-11-18T06:36:00ZEvolutionary systems biology of amino acid biosynthetic cost in yeast.1932-620310.1371/journal.pone.0011935https://doaj.org/article/12202ad9fd7b41cfb56b0f6a1e8ae7482010-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20808905/?tool=EBIhttps://doaj.org/toc/1932-6203Every protein has a biosynthetic cost to the cell based on the synthesis of its constituent amino acids. In order to optimise growth and reproduction, natural selection is expected, where possible, to favour the use of proteins whose constituents are cheaper to produce, as reduced biosynthetic cost may confer a fitness advantage to the organism. Quantifying the cost of amino acid biosynthesis presents challenges, since energetic requirements may change across different cellular and environmental conditions. We developed a systems biology approach to estimate the cost of amino acid synthesis based on genome-scale metabolic models and investigated the effects of the cost of amino acid synthesis on Saccharomyces cerevisiae gene expression and protein evolution. First, we used our two new and six previously reported measures of amino acid cost in conjunction with codon usage bias, tRNA gene number and atomic composition to identify which of these factors best predict transcript and protein levels. Second, we compared amino acid cost with rates of amino acid substitution across four species in the genus Saccharomyces. Regardless of which cost measure is used, amino acid biosynthetic cost is weakly associated with transcript and protein levels. In contrast, we find that biosynthetic cost and amino acid substitution rates show a negative correlation, but for only a subset of cost measures. In the economy of the yeast cell, we find that the cost of amino acid synthesis plays a limited role in shaping transcript and protein expression levels compared to that of translational optimisation. Biosynthetic cost does, however, appear to affect rates of amino acid evolution in Saccharomyces, suggesting that expensive amino acids may only be used when they have specific structural or functional roles in protein sequences. However, as there appears to be no single currency to compute the cost of amino acid synthesis across all cellular and environmental conditions, we conclude that a systems approach is necessary to unravel the full effects of amino acid biosynthetic cost in complex biological systems.Michael D BartonDaniela DelneriStephen G OliverMagnus RattrayCasey M BergmanPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 5, Iss 8, p e11935 (2010)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Michael D Barton Daniela Delneri Stephen G Oliver Magnus Rattray Casey M Bergman Evolutionary systems biology of amino acid biosynthetic cost in yeast.
description	Every protein has a biosynthetic cost to the cell based on the synthesis of its constituent amino acids. In order to optimise growth and reproduction, natural selection is expected, where possible, to favour the use of proteins whose constituents are cheaper to produce, as reduced biosynthetic cost may confer a fitness advantage to the organism. Quantifying the cost of amino acid biosynthesis presents challenges, since energetic requirements may change across different cellular and environmental conditions. We developed a systems biology approach to estimate the cost of amino acid synthesis based on genome-scale metabolic models and investigated the effects of the cost of amino acid synthesis on Saccharomyces cerevisiae gene expression and protein evolution. First, we used our two new and six previously reported measures of amino acid cost in conjunction with codon usage bias, tRNA gene number and atomic composition to identify which of these factors best predict transcript and protein levels. Second, we compared amino acid cost with rates of amino acid substitution across four species in the genus Saccharomyces. Regardless of which cost measure is used, amino acid biosynthetic cost is weakly associated with transcript and protein levels. In contrast, we find that biosynthetic cost and amino acid substitution rates show a negative correlation, but for only a subset of cost measures. In the economy of the yeast cell, we find that the cost of amino acid synthesis plays a limited role in shaping transcript and protein expression levels compared to that of translational optimisation. Biosynthetic cost does, however, appear to affect rates of amino acid evolution in Saccharomyces, suggesting that expensive amino acids may only be used when they have specific structural or functional roles in protein sequences. However, as there appears to be no single currency to compute the cost of amino acid synthesis across all cellular and environmental conditions, we conclude that a systems approach is necessary to unravel the full effects of amino acid biosynthetic cost in complex biological systems.
format	article
author	Michael D Barton Daniela Delneri Stephen G Oliver Magnus Rattray Casey M Bergman
author_facet	Michael D Barton Daniela Delneri Stephen G Oliver Magnus Rattray Casey M Bergman
author_sort	Michael D Barton
title	Evolutionary systems biology of amino acid biosynthetic cost in yeast.
title_short	Evolutionary systems biology of amino acid biosynthetic cost in yeast.
title_full	Evolutionary systems biology of amino acid biosynthetic cost in yeast.
title_fullStr	Evolutionary systems biology of amino acid biosynthetic cost in yeast.
title_full_unstemmed	Evolutionary systems biology of amino acid biosynthetic cost in yeast.
title_sort	evolutionary systems biology of amino acid biosynthetic cost in yeast.
publisher	Public Library of Science (PLoS)
publishDate	2010
url	https://doaj.org/article/12202ad9fd7b41cfb56b0f6a1e8ae748
work_keys_str_mv	AT michaeldbarton evolutionarysystemsbiologyofaminoacidbiosyntheticcostinyeast AT danieladelneri evolutionarysystemsbiologyofaminoacidbiosyntheticcostinyeast AT stephengoliver evolutionarysystemsbiologyofaminoacidbiosyntheticcostinyeast AT magnusrattray evolutionarysystemsbiologyofaminoacidbiosyntheticcostinyeast AT caseymbergman evolutionarysystemsbiologyofaminoacidbiosyntheticcostinyeast
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Evolutionary systems biology of amino acid biosynthetic cost in yeast.

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