Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins

Abstract

Protein evolution is not simply a race toward improved function. Because organisms compete for limited resources, fitness is also affected by the relative economy of an organism’s proteome. Indeed, many abundant proteins contain relatively high percentages of amino acids that are metabolically less taxing for the cell to make, thus reducing cellular cost. However, not all abundant proteins are economical, and many economical proteins are not particularly abundant. Here we examined protein composition and found that the relative synthetic cost of amino acids constrains the composition of microbial extracellular proteins. In Escherichia coli, extracellular proteins contain, on average, fewer energetically expensive amino acids independent of their abundance, length, function, or structure. Economic pressures have strategically shaped the amino acid composition of multicomponent surface appendages, such as flagella, curli, and type I pili, and extracellular enzymes, including type III effector proteins and secreted serine proteases. Furthermore, in silico analysis of Pseudomonas syringae, Mycobacterium tuberculosis, Saccharomyces cerevisiae, and over 25 other microbes spanning a wide range of GC content revealed a broad bias toward more economical amino acids in extracellular proteins. The synthesis of any protein, especially those rich in expensive aromatic amino acids, represents a significant investment. Because extracellular proteins are lost to the environment and not recycled like other cellular proteins, they present a greater burden on the cell, as their amino acids cannot be reutilized during translation. We hypothesize that evolution has optimized extracellular proteins to reduce their synthetic burden on the cell.

The AlternativeTranslational Profile That Underlies the Immune-Evasive State of Persistence in Chlamydiaceae Exploits Differential Tryptophan Contents of the Protein Repertoire

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Bistable Expression of CsgD in Salmonella enterica Serovar Typhimurium Connects Virulence to Persistence

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Expression profiles of growth hormone receptor and insulin-like growth factor I in cattle and yak tissues revealed by quantitative real-time PCR

“…Under normal physiological conditions, the synthesis of any component of the organism should be equal to the amount of it required (Smith & Chapman 2010), so translational and transcript levels for most of the genes should be equal too. Meanwhile, decreased serum IGF-I is related to reduced liver IGF-I mRNA in food-deprived cattle (Wang et al 2003).…”