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 metabolica...

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Autores principales:	Daniel R. Smith, Matthew R. Chapman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2010
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/afb317ebba604a36b802314583e3f57d
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spelling	oai:doaj.org-article:afb317ebba604a36b802314583e3f57d2021-11-15T15:38:16ZEconomical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins10.1128/mBio.00131-102150-7511https://doaj.org/article/afb317ebba604a36b802314583e3f57d2010-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00131-10https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Microbes secrete proteins to perform essential interactions with their environment, such as motility, pathogenesis, biofilm formation, and resource acquisition. However, because microbes generally lack protein import systems, secretion is often a one-way street. Consequently, secreted proteins are less likely to be recycled by the cell due to environmental loss. We demonstrate that evolution has in turn selected these extracellular proteins for increased economy at the level of their amino acid composition. Compared to their cellular counterparts, extracellular proteins have fewer synthetically expensive amino acids and more inexpensive amino acids. The resulting bias lessens the loss of cellular resources due to secretion. Furthermore, this economical bias was observed regardless of the abundance, length, structure, or function of extracellular proteins. Thus, it appears that economy may address the compositional bias seen in many extracellular proteins and deliver further insight into the forces driving their evolution.Daniel R. SmithMatthew R. ChapmanAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 1, Iss 3 (2010)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Daniel R. Smith Matthew R. Chapman Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
description	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. IMPORTANCE Microbes secrete proteins to perform essential interactions with their environment, such as motility, pathogenesis, biofilm formation, and resource acquisition. However, because microbes generally lack protein import systems, secretion is often a one-way street. Consequently, secreted proteins are less likely to be recycled by the cell due to environmental loss. We demonstrate that evolution has in turn selected these extracellular proteins for increased economy at the level of their amino acid composition. Compared to their cellular counterparts, extracellular proteins have fewer synthetically expensive amino acids and more inexpensive amino acids. The resulting bias lessens the loss of cellular resources due to secretion. Furthermore, this economical bias was observed regardless of the abundance, length, structure, or function of extracellular proteins. Thus, it appears that economy may address the compositional bias seen in many extracellular proteins and deliver further insight into the forces driving their evolution.
format	article
author	Daniel R. Smith Matthew R. Chapman
author_facet	Daniel R. Smith Matthew R. Chapman
author_sort	Daniel R. Smith
title	Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
title_short	Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
title_full	Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
title_fullStr	Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
title_full_unstemmed	Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins
title_sort	economical evolution: microbes reduce the synthetic cost of extracellular proteins
publisher	American Society for Microbiology
publishDate	2010
url	https://doaj.org/article/afb317ebba604a36b802314583e3f57d
work_keys_str_mv	AT danielrsmith economicalevolutionmicrobesreducethesyntheticcostofextracellularproteins AT matthewrchapman economicalevolutionmicrobesreducethesyntheticcostofextracellularproteins
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Economical Evolution: Microbes Reduce the Synthetic Cost of Extracellular Proteins

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