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Title: A Comparison of the Costs and Benefits of Bacterial Gene Expression

In order to study how a bacterium allocates its resources, we compared the costs and benefits of most (86%) of the proteins in Escherichia coli K-12 during growth in minimal glucose medium. The cost or investment in each protein was estimated from ribosomal profiling data, and the benefit of each protein was measured by assaying a library of transposon mutants. We found that proteins that are important for fitness are usually highly expressed, and 95% of these proteins are expressed at above 13 parts per million (ppm). Conversely, proteins that do not measurably benefit the host (with a benefit of less than 5% per generation) tend to be weakly expressed, with a median expression of 13 ppm. In aggregate, genes with no detectable benefit account for 31% of protein production, or about 22% if we correct for genetic redundancy. Though some of the apparently unnecessary expression could have subtle benefits in minimal glucose medium, the majority of the burden is due to genes that are important in other conditions. We propose that at least 13% of the cell's protein is on standby in case conditions change.
Authors:
ORCiD logo [1] ;  [1] ;  [1] ;  [1] ;  [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of Wisconsin, Madison, WI (United States)
Publication Date:
Grant/Contract Number:
AC02-05CH11231
Type:
Published Article
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 10; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES
OSTI Identifier:
1338429
Alternate Identifier(s):
OSTI ID: 1377509

Price, Morgan N., Wetmore, Kelly M., Deutschbauer, Adam M., Arkin, Adam P., and Pfleger, Brian Frederick. A Comparison of the Costs and Benefits of Bacterial Gene Expression. United States: N. p., Web. doi:10.1371/journal.pone.0164314.
Price, Morgan N., Wetmore, Kelly M., Deutschbauer, Adam M., Arkin, Adam P., & Pfleger, Brian Frederick. A Comparison of the Costs and Benefits of Bacterial Gene Expression. United States. doi:10.1371/journal.pone.0164314.
Price, Morgan N., Wetmore, Kelly M., Deutschbauer, Adam M., Arkin, Adam P., and Pfleger, Brian Frederick. 2016. "A Comparison of the Costs and Benefits of Bacterial Gene Expression". United States. doi:10.1371/journal.pone.0164314.
@article{osti_1338429,
title = {A Comparison of the Costs and Benefits of Bacterial Gene Expression},
author = {Price, Morgan N. and Wetmore, Kelly M. and Deutschbauer, Adam M. and Arkin, Adam P. and Pfleger, Brian Frederick},
abstractNote = {In order to study how a bacterium allocates its resources, we compared the costs and benefits of most (86%) of the proteins in Escherichia coli K-12 during growth in minimal glucose medium. The cost or investment in each protein was estimated from ribosomal profiling data, and the benefit of each protein was measured by assaying a library of transposon mutants. We found that proteins that are important for fitness are usually highly expressed, and 95% of these proteins are expressed at above 13 parts per million (ppm). Conversely, proteins that do not measurably benefit the host (with a benefit of less than 5% per generation) tend to be weakly expressed, with a median expression of 13 ppm. In aggregate, genes with no detectable benefit account for 31% of protein production, or about 22% if we correct for genetic redundancy. Though some of the apparently unnecessary expression could have subtle benefits in minimal glucose medium, the majority of the burden is due to genes that are important in other conditions. We propose that at least 13% of the cell's protein is on standby in case conditions change.},
doi = {10.1371/journal.pone.0164314},
journal = {PLoS ONE},
number = 10,
volume = 11,
place = {United States},
year = {2016},
month = {10}
}

Works referenced in this record:

Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants the Keio collection
journal, February 2006
  • Baba, Tomoya; Ara, Takeshi; Hasegawa, Miki
  • Molecular Systems Biology, Vol. 2, Article No. 2006.0008
  • DOI: 10.1038/msb4100050

Rapid Quantification of Mutant Fitness in Diverse Bacteria by Sequencing Randomly Bar-Coded Transposons
journal, May 2015
  • Wetmore, Kelly M.; Price, Morgan N.; Waters, Robert J.
  • mBio, Vol. 6, Issue 3, Article No. e00306-15
  • DOI: 10.1128/mBio.00306-15

Emergent Properties of Reduced-Genome Escherichia coli
journal, May 2006
  • Posfai, G.; Plunkett III, Guy; Feh�r, Tam�s
  • Science, Vol. 312, Issue 5776, p. 1044-1046
  • DOI: 10.1126/science.1126439

The Soluble and Membrane-bound Transhydrogenases UdhA and PntAB Have Divergent Functions in NADPH Metabolism of Escherichia coli
journal, December 2003
  • Sauer, Uwe; Canonaco, Fabrizio; Heri, Sylvia
  • Journal of Biological Chemistry, Vol. 279, Issue 8, p. 6613-6619
  • DOI: 10.1074/jbc.M311657200