1887

Abstract

Micro-organisms often face multiple stresses in natural habitats. Individual stresses are well known to influence mutation rates and the spectra of mutational types, but the extent to which multiple stresses affect the genetic variation in populations is unknown. Here we investigate pair-wise combinations of nutritional stresses in Escherichia coli to determine their effect on mutation rates and mutational types. Environmental interactions modified both the rate and spectrum of mutations in double-limited environments, but the effects were not additive or synergistic relative to single stresses. Generally, bacteria in the mixed environments behaved as if one of the two single-stress stimuli was more dominant and the genetic variation seen with every dual limitation was intermediate between known patterns with individual stresses. The composition of mutational types with double stresses was also intermediate between individual stress patterns. At least with mutations, the single stressor results available are reasonable indicators of stress-induced genetic variation in multifaceted natural habitats. With the influence of 11 conditions available on mutational patterns, we can now also see the clustering of mutational types as a function of these environments.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000727
2018-10-05
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/12/1491.html?itemId=/content/journal/micro/10.1099/mic.0.000727&mimeType=html&fmt=ahah

References

  1. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V et al. Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 2010; 408:3746–3762 [View Article][PubMed]
    [Google Scholar]
  2. Egli T, Zinn M. The concept of multiple-nutrient-limited growth of microorganisms and its application in biotechnological processes. Biotechnol Adv 2003; 22:35–43 [View Article][PubMed]
    [Google Scholar]
  3. Liess M, Foit K, Knillmann S, Schäfer RB, Liess HD. Predicting the synergy of multiple stress effects. Sci Rep 2016; 6:32965 [View Article][PubMed]
    [Google Scholar]
  4. Browning TJ, Achterberg EP, Rapp I, Engel A, Bertrand EM et al. Nutrient co-limitation at the boundary of an oceanic gyre. Nature 2017; 551:242–246 [View Article][PubMed]
    [Google Scholar]
  5. Al Mamun AA, Lombardo MJ, Shee C, Lisewski AM, Gonzalez C et al. Identity and function of a large gene network underlying mutagenic repair of DNA breaks. Science 2012; 338:1344–1348 [View Article][PubMed]
    [Google Scholar]
  6. Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A et al. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat Commun 2013; 4:1610 [View Article][PubMed]
    [Google Scholar]
  7. Eisen JA, Hanawalt PC. A phylogenomic study of DNA repair genes, proteins, and processes. Mutat Res 1999; 435:171–213 [View Article][PubMed]
    [Google Scholar]
  8. Lovett ST. The DNA Damage Response. In Storz G, Hengge R. (editors) Bacterial Stress Responses, 2nd ed. 2011 pp. 205–228
    [Google Scholar]
  9. Maharjan RP, Ferenci T. A shifting mutational landscape in 6 nutritional states: Stress-induced mutagenesis as a series of distinct stress input-mutation output relationships. PLoS Biol 2017; 15:e2001477 [View Article][PubMed]
    [Google Scholar]
  10. Maharjan RP, Ferenci T. The impact of growth rate and environmental factors on mutation rates and spectra in Escherichia coli. Environ Microbiol Rep 2018 [View Article][PubMed]
    [Google Scholar]
  11. Foster PL. Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 2007; 42:373–397 [View Article][PubMed]
    [Google Scholar]
  12. Galhardo RS, Hastings PJ, Rosenberg SM. Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol Biol 2007; 42:399–435 [View Article][PubMed]
    [Google Scholar]
  13. Bjedov I, Tenaillon O, Gérard B, Souza V, Denamur E et al. Stress-induced mutagenesis in bacteria. Science 2003; 300:1404–1409 [View Article][PubMed]
    [Google Scholar]
  14. Gibson JL, Lombardo MJ, Thornton PC, Hu KH, Galhardo RS et al. The sigma(E) stress response is required for stress-induced mutation and amplification in Escherichia coli. Mol Microbiol 2010; 77:415–430 [View Article][PubMed]
    [Google Scholar]
  15. Fitzgerald DM, Hastings PJ, Rosenberg SM. Stress-induced mutagenesis: implications in cancer and drug resistance. Annu Rev Cancer Biol 2017; 1:119–140 [View Article][PubMed]
    [Google Scholar]
  16. Denamur E, Matic I. Evolution of mutation rates in bacteria. Mol Microbiol 2006; 60:820–827 [View Article][PubMed]
    [Google Scholar]
  17. Giraud A, Matic I, Radman M, Fons M, Taddei F. Mutator bacteria as a risk factor in treatment of infectious diseases. Antimicrob Agents Chemother 2002; 46:863–865 [View Article][PubMed]
    [Google Scholar]
  18. Warsi OM, Dykhuizen DE. Evolutionary implications of Liebig's law of the minimum: selection under low concentrations of two nonsubstitutable nutrients. Ecol Evol 2017; 7:5296–5309 [View Article][PubMed]
    [Google Scholar]
  19. Karve SM, Bhave D, Nevgi D, Dey S. Escherichia coli populations adapt to complex, unpredictable fluctuations by minimizing trade-offs across environments. J Evol Biol 2016; 29:2545–2555 [View Article][PubMed]
    [Google Scholar]
  20. Ferenci T, Zhou Z, Betteridge T, Ren Y, Liu Y et al. Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol 2009; 191:4025–4029 [View Article][PubMed]
    [Google Scholar]
  21. Miller J. Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1972
    [Google Scholar]
  22. Wang L, Spira B, Zhou Z, Feng L, Maharjan RP et al. Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2010; 2:478–487 [View Article][PubMed]
    [Google Scholar]
  23. Atlan D, Portalier R. Purification of extracellular alkaline phosphatase released by Escherichia coli excretory mutants. Appl Microbiol Biotechnol 1987; 26:318–322 [View Article]
    [Google Scholar]
  24. Luria SE, Delbrück M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 1943; 28:491–511[PubMed]
    [Google Scholar]
  25. Hall BG. Adaptive evolution that requires multiple spontaneous mutations. I. Mutations involving an insertion sequence. Genetics 1988; 120:887–897[PubMed]
    [Google Scholar]
  26. Maharjan R, Ferenci T. Mutational signatures indicative of environmental stress in bacteria. Mol Biol Evol 2015; 32:380–391 [View Article][PubMed]
    [Google Scholar]
  27. Sarkar S, Ma WT, Sandri GH. On fluctuation analysis: a new, simple and efficient method for computing the expected number of mutants. Genetica 1992; 85:173–179 [View Article][PubMed]
    [Google Scholar]
  28. Hall BM, Ma CX, Liang P, Singh KK. Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 2009; 25:1564–1565 [View Article][PubMed]
    [Google Scholar]
  29. Hammer O, Harper DAT, Ryan PD. PAST: Palaeontological Statistics software package for education and data analysis. Palaeontologica Electronica 2001; 4:9
    [Google Scholar]
  30. Spira B, Ferenci T. Alkaline phosphatase as a reporter of σS levels and rpoS polymorphisms in different E. coli strains. Arch Microbiol 2008; 189:43–47 [View Article][PubMed]
    [Google Scholar]
  31. Fehér T, Cseh B, Umenhoffer K, Karcagi I, Pósfai G. Characterization of cycA mutants of Escherichia coli. An assay for measuring in vivo mutation rates. Mutat Res 2006; 595:184–190 [View Article][PubMed]
    [Google Scholar]
  32. Sakai A, Nakanishi M, Yoshiyama K, Maki H. Impact of reactive oxygen species on spontaneous mutagenesis in Escherichia coli. Genes Cells 2006; 11:767–778 [View Article][PubMed]
    [Google Scholar]
  33. Shewaramani S, Finn TJ, Leahy SC, Kassen R, Rainey PB et al. Anaerobically grown Escherichia coli has an enhanced mutation rate and distinct mutational spectra. PLoS Genet 2017; 13:e1006570 [View Article][PubMed]
    [Google Scholar]
  34. Maharjan R, Ferenci T. Stress-induced mutation rates show a sigmoidal and saturable increase due to the RpoS sigma factor in Escherichia coli. Genetics 2014; 198:1231–1235 [View Article][PubMed]
    [Google Scholar]
  35. Merrikh H, Ferrazzoli AE, Bougdour A, Olivier-Mason A, Lovett ST. A DNA damage response in Escherichia coli involving the alternative sigma factor, RpoS. Proc Natl Acad Sci USA 2009; 106:611–616 [View Article][PubMed]
    [Google Scholar]
  36. Saint-Ruf C, Pesut J, Sopta M, Matic I. Causes and consequences of DNA repair activity modulation during stationary phase in Escherichia coli. Crit Rev Biochem Mol Biol 2007; 42:259–270 [View Article][PubMed]
    [Google Scholar]
  37. Tsui HC, Feng G, Winkler ME. Negative regulation of mutS and mutH repair gene expression by the Hfq and RpoS global regulators of Escherichia coli K-12. J Bacteriol 1997; 179:7476–7487 [View Article][PubMed]
    [Google Scholar]
  38. King T, Ferenci T. Divergent roles of RpoS in Escherichia coli under aerobic and anaerobic conditions. FEMS Microbiol Lett 2005; 244:323–327 [View Article][PubMed]
    [Google Scholar]
  39. Ferenci T, Maharjan R. Mutational heterogeneity: A key ingredient of bet-hedging and evolutionary divergence?. Bioessays 2015; 37:123–130 [View Article]
    [Google Scholar]
  40. Hooker HD. Liebig's law of the minimum in relation to general biological problems. Science 1917; 46:197–204 [View Article][PubMed]
    [Google Scholar]
  41. Walworth NG, Fu FX, Webb EA, Saito MA, Moran D et al. Mechanisms of increased Trichodesmium fitness under iron and phosphorus co-limitation in the present and future ocean. Nat Commun 2016; 7:12081 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000727
Loading
/content/journal/micro/10.1099/mic.0.000727
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error