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The fitness effects of a point mutation in Escherichia coli change with founding population density

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Abstract

Although intraspecific competition plays a seminal role in organismal evolution, little is known about the fitness effects of mutations at different population densities. We identified a point mutation in the cyclic AMP receptor protein (CRP) gene in Escherichia coli that confers significantly higher fitness than the wildtype at low founding population density, but significantly lower fitness at high founding density. Because CRP is a transcription factor that regulates the expression of nearly 500 genes, we compared global gene expression profiles of the mutant and wildtype strains. This mutation (S63F) does not affect expression of crp itself, but it does significantly affect expression of 170 and 157 genes at high and low founding density, respectively. Interestingly, acid resistance genes, some of which are known to exhibit density-dependent effects in E. coli, were consistently differentially expressed at high but not low density. As such, these genes may play a key role in reducing the crp mutant’s fitness at high density, although other differentially expressed genes almost certainly also contribute to the fluctuating fitness differences we observed. Whatever the causes, we suspect that many mutations may exhibit density-dependent fitness effects in natural populations, so the fate of new mutations may frequently depend on the effective population size when they originate.

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References

  • Adler J, Templeton B (1967) The effect of environmental conditions on the motility of Escherichia coli. J Gen Microbiol 46:175–184

    Article  CAS  PubMed  Google Scholar 

  • Agilent Technologies Inc (2010) GeneSpring software. Agilent Technologies, Santa Clara

    Google Scholar 

  • Bederson BB, Shneiderman B, Wattenberg M (2002) Ordered and quantum treemaps: making effective use of 2D space to display hierarchies. ACM Trans Graph 21:833–854

    Article  Google Scholar 

  • Busby S, Ebright RH (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293:199–213

    Article  CAS  PubMed  Google Scholar 

  • Castanie-Cornet M-P, Penfound TA, Smith D, Elliott JF, Foster JW (1999) Control of acid resistance in Escherichia coli. J Bacteriol 181:3525–3535

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chang S-M, Shaw RG (2003) The contribution of spontaneous mutation to variation in environmental response in Arabidopsis thaliana: responses to nutrients. Evolution 57:984–994

    Article  PubMed  Google Scholar 

  • Claret L, Hughes C (2002) Interaction of the atypical prokaryotic transcription activator FlhD2C2 with early promoters of the flagellar gene hierarchy. J Mol Biol 321:185–199

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1859) The origin of species. John Murray, London

    Google Scholar 

  • Datta S, Costantino N, Court DL (2006) A set of recombineering plasmids for gram-negative bacteria. Gene 379:109–115

    Article  CAS  PubMed  Google Scholar 

  • De Biase D, Tramonti A, Bossa F, Visca P (1999) The response to stationary-phase stress conditions in Escherichia coli: role and regulation of the glutamic acid decarboxylase system. Mol Microbiol 32:1198–1211

    Article  PubMed  Google Scholar 

  • de Visser JAGM, Cooper TF, Elena SF (2011) The causes of epistasis. Proc R Soc Lond B 278:3617–3624

    Article  Google Scholar 

  • Desai MM, Fisher DS, Murray AW (2007) The speed of evolution and maintenance of variation in asexual populations. Curr Biol 17:385–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards RJ, Sockett RE, Brookfield JFY (2002) A simple method for genome-wide screening for advantageous insertions of mobile DNAs in Escherichia coli. Curr Biol 12:863–867

    Article  CAS  PubMed  Google Scholar 

  • Engen S, Lande R, Sæther B-E (2009) Fixation probability of beneficial mutations in a fluctuating population. Genet Res 91:73–82

    Article  Google Scholar 

  • Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fry JD, Heinsohn SL (2002) Environment dependence of mutational parameters for viability in Drosophila melanogaster. Genetics 161:1155–1167

    PubMed  PubMed Central  Google Scholar 

  • Gerrish PJ, Lenski RE (1998) The fate of competing beneficial mutations in an asexual population. Genetica 102(103):127–144

    Article  PubMed  Google Scholar 

  • Hommais F, Krin E, Coppée J-Y, Lacroix C, Yeramian E, Danchin A, Bertin P (2004) GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150:61–72

    Article  CAS  PubMed  Google Scholar 

  • Houchmandzadeh B, Vallade M (2011) The fixation probability of a beneficial mutation in a geographically structured population. New J Phys 13:073020

    Article  Google Scholar 

  • Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13

    Article  Google Scholar 

  • IBM Corp. (2013) IBM SPSS statistics for windows. IBM Corp, Armonk

    Google Scholar 

  • Kang Y, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR (2004) Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186:4921–4930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kao KC, Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40:1499–1504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keseler IM, Collado-Vides J, Santos-Zavaleta A, Peralta-Gil M, Gama-Castro S, Muñiz-Rascado L, Bonavides-Martinez C, Paley S, Krummenacker M, Altman T, Kaipa P, Spaulding A, Pacheco J, Latendresse M, Fulcher C, Sarker M, Shearer AG, Mackie A, Paulsen I, Gunsalus RP, Karp PD (2011) EcoCyc: a comprehensive database of Escherichia coli biology. Nucleic Acids Res 39:D583–D590

    Article  CAS  PubMed  Google Scholar 

  • Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunsalus RP, Paulsen I, Karp PD (2013) EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:D605–D612

    Article  CAS  PubMed  Google Scholar 

  • Kimura M (1962) On the probability of fixation of mutant genes in a population. Genetics 47:713–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kolb A, Busby S, Buc II, Garges S, Adhya S (1993) Transcriptional regulation by cAMP and its receptor protein. Annu Rev Biochem 62:749–797

    Article  CAS  PubMed  Google Scholar 

  • Korona R (1999) Genetic load of the yeast Saccharomyces cerevisiae under diverse environmental conditions. Evolution 53:1966–1971

    Article  Google Scholar 

  • Lenski RE, Rose MR, Simpson SE, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. Am Nat 138:1315–1341

    Article  Google Scholar 

  • Lind PA, Berg OG, Andersson DI (2010) Mutational robustness of ribosomal protein genes. Science 330:825–827

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Blanchard J, Houle D, Kibota T, Schultz S, Vassilieva L, Willis J (1999) Perspective: spontaneous deleterious mutation. Evolution 53:645–663

    Article  Google Scholar 

  • Ma Z, Richard H, Tucker DL, Conway T, Foster JW (2002) Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J Bacteriol 184:7001–7012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Z, Richard H, Foster JW (2003) pH-dependent modulation of cyclic AMP levels and GadW-dependent repression of RpoS affect synthesis of the GadX regulator and Escherichia coli acid resistance. J Bacteriol 185:6852–6859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin G, Lenormand T (2006) The fitness effect of mutations across environments: a survey in light of fitness landscape models. Evolution 60:2413–2427

    Article  PubMed  Google Scholar 

  • Mates AK, Sayed AK, Foster JW (2007) Products of the Escherichia coli acid fitness island attenuate metabolite stress at extremely low pH and mediate a cell density-dependent acid resistance. J Bacteriol 189:2759–2768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKay DB, Weber IT, Steitz TA (1982) Structure of catabolite gene activator protein at 2.9-A resolution. Incorporation of amino acid sequence and interactions with cyclic AMP. J Biol Chem 257:9518–9524

    CAS  PubMed  Google Scholar 

  • Miller J (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199

    Article  CAS  PubMed  Google Scholar 

  • Mira A, Moran NA (2002) Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol 44:137–143

    Article  CAS  PubMed  Google Scholar 

  • Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633

    Article  CAS  PubMed  Google Scholar 

  • Mueller LD (1997) Theoretical and empirical examination of density-dependent selection. Annu Rev Ecol Syst 28:269–288

    Article  Google Scholar 

  • Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119:736–747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Novella IS, Reissig DD, Wilke CO (2004) Density-dependent selection in vesicular stomatitis virus. J Virol 78:5799–5804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochman H, Wilson AC (1987) Evolutionary history of enteric bacteria. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, pp 1649–1654

    Google Scholar 

  • Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98

    Article  CAS  PubMed  Google Scholar 

  • Patwa Z, Wahl LM (2008) The fixation probability of beneficial mutations. J R Soc Interface 5:1279–1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plague GR, Dougherty KM, Boodram KS, Boustani SE, Cao H, Manning SR, McNally CC (2011) Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli. Genetica 139:895–902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Sharp NP, Agrawal AF (2008) Mating density and the strength of sexual selection against deleterious alleles in Drosophila melanogaster. Evolution 62:857–867

    Article  PubMed  Google Scholar 

  • Shin S, Park C (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177:4696–4702

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silverman M, Simon M (1974) Characterization of Escherichia coli flagellar mutants that are insensitive to catabolite repression. J Bacteriol 120:1196–1203

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sperandio V, Torres AG, Kaper JB (2002) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809–821

    Article  CAS  PubMed  Google Scholar 

  • Stafford GP, Ogi T, Hughes C (2005) Binding and transcriptional activation of non-flagellar genes by the Escherichia coli flagellar master regulator FlhD2C2. Microbiology 151:1779–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stoebel DM, Dean AM, Dykhuizen DE (2008) The cost of expression of Escherichia coli lac operon proteins is in the process, not in the product. Genetics 178:1653–1660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomason L, Court DL, Bubunenko M, Costantino N, Wilson H, Datta S, Oppenheim A (2007) Recombineering: genetic engineering in bacteria using homologous recombination. Curr Protoc Mol Biol 78(1):16.11–16.24

    Google Scholar 

  • Travis J, Leips J, Rodd FH (2013) Evolution in population parameters: density-dependent selection or density-dependent fitness? Am Nat 181:S9–S20

    Article  PubMed  Google Scholar 

  • Vasi F, Travisano M, Lenski RE (1994) Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am Nat 144:432–456

    Article  Google Scholar 

  • Wahl LM, Gerrish PJ (2001) The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55:2606–2610

    Article  CAS  PubMed  Google Scholar 

  • Waxman D (2011) A unified treatment of the probability of fixation when population size and the strength of selection change over time. Genetics 188:907–913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinreich DM, Delaney NF, DePristo MA, Hartl DL (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111–114

    Article  CAS  PubMed  Google Scholar 

  • Yokota T, Gots JS (1970) Requirement of adenosine 3’, 5’-cyclic phosphate for flagella formation in Escherichia coli and Salmonella typhimurium. J Bacteriol 103:513–516

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We thank Kevin Dougherty and Evelyn Fetridge for insightful discussion, Yaping Yang for assistance in the lab, Dr. Yajun Yan for use of his lab for the growth curve measurements, and the anonymous reviewers for critically reviewing the manuscript. This study was funded by the National Institutes of Health (Grant Number 7R15GM081862-02 awarded to G.R.P.).

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Correspondence to Gordon R. Plague.

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Cao, H., Plague, G.R. The fitness effects of a point mutation in Escherichia coli change with founding population density. Genetica 144, 417–424 (2016). https://doi.org/10.1007/s10709-016-9910-5

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