#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments


Changing environmental conditions are the norm in biology. However, understanding adaptation to complex environments presents many challenges. For example, adaptation to resource-rich environments can potentially have many successful evolutionary trajectories to increased fitness. Even in conditions of plenty, the utilization of numerous but novel resources can require multiple mutations before a benefit is accrued. We evolved two bacterial species isolated from the gut of healthy humans in two different, resource-rich media commonly used in the laboratory. We anticipated that under weak selection the population would evolve tremendous genetic diversity. Despite such a complex genetic background we were able to identify a strong degree of parallel evolution and using a combination of population proteomic and population genomic approaches we show that two global regulators, arcA and rpoS, are the principle targets of selection. Up-regulation of the different metabolic pathways that are controlled by these global regulators in combination with up-regulation of transporters that transport nutrients into the cell revealed increased use of the novel resources. Thus global regulators can provide a one-step model to shift metabolism efficiently and provide rapid a one-step reprogramming of the cell metabolic profile.


Vyšlo v časopise: Mutations in Global Regulators Lead to Metabolic Selection during Adaptation to Complex Environments. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004872
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004872

Souhrn

Changing environmental conditions are the norm in biology. However, understanding adaptation to complex environments presents many challenges. For example, adaptation to resource-rich environments can potentially have many successful evolutionary trajectories to increased fitness. Even in conditions of plenty, the utilization of numerous but novel resources can require multiple mutations before a benefit is accrued. We evolved two bacterial species isolated from the gut of healthy humans in two different, resource-rich media commonly used in the laboratory. We anticipated that under weak selection the population would evolve tremendous genetic diversity. Despite such a complex genetic background we were able to identify a strong degree of parallel evolution and using a combination of population proteomic and population genomic approaches we show that two global regulators, arcA and rpoS, are the principle targets of selection. Up-regulation of the different metabolic pathways that are controlled by these global regulators in combination with up-regulation of transporters that transport nutrients into the cell revealed increased use of the novel resources. Thus global regulators can provide a one-step model to shift metabolism efficiently and provide rapid a one-step reprogramming of the cell metabolic profile.


Zdroje

1. LandeR (1983) The Response to Selection on Major and Minor Mutations Affecting a Metrical Trait. Heredity 50: 47–65.

2. CooperVS, LenskiRE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.

3. LeibyN, MarxCJ (2014) Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biol 12: e1001789.

4. PengL, ShimizuK (2003) Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement. Appl Microbiol Biotechnol 61: 163–178.

5. FutuymaDJ, MorenoG (1988) The Evolution of Ecological Specialization. Annual Review of Ecology and Systematics 19: 207–233.

6. BarrickJE, LenskiRE (2009) Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harbor symposia on quantitative biology 74: 119–129.

7. ElenaSF, LenskiRE (2003) Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nature Reviews Genetics 4: 457–469.

8. LenskiRE, RoseMR, SimpsonSC, TadlerSC (1991) Long-term experimental evolution in Escherichia coli I: Adaptation and divergence during 2,000 generations. American Naturalist 138: 1315–1341.

9. LenskiRE, TravisanoM (1994) Dynamics of adaptation and diversification: A 10,000-generation experiment with bacterial populations. Proceedings of the National Academy of Sciences of the United States of America 91: 6808–6814.

10. SaxerG, DoebeliM, TravisanoM (2009) Spatial structure leads to ecological breakdown and loss of diversity. Proceedings of the Royal Society B-Biological Sciences 276: 2065–2070.

11. SaxerG, DoebeliM, TravisanoM (2010) The Repeatability of Adaptive Radiation During Long- Term Experimental Evolution of Escherichia coli in a Multiple Nutrient Environment Plos One. 5: e14184.

12. MillerC, KongJY, TranTT, AriasCA, SaxerG, et al. (2013) Adaptation of Enterococcus faecalis to Daptomycin Reveals an Ordered Progression to Resistance. Antimicrobial Agents and Chemotherapy 57: 5373–5383.

13. ToprakE, VeresA, MichelJB, ChaitR, HartlDL, et al. (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nature Genetics 44: 101–U140.

14. CounagoR, WilsonCJ, PenaMI, Wittung-StafshedeP, ShamooY (2008) An adaptive mutation in adenylate kinase that increases organismal fitness is linked to stability-activity trade-offs. Protein Engineering Design & Selection 21: 19–27.

15. TenaillonO, Rodriguez-VerdugoA, GautRL, McDonaldP, BennettAF, et al. (2012) The Molecular Diversity of Adaptive Convergence. Science 335: 457–461.

16. ChouHH, ChiuHC, DelaneyNF, SegreD, MarxCJ (2011) Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation. Science 332: 1190–1192.

17. KhanAI, DinhDM, SchneiderD, LenskiRE, CooperTF (2011) Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population. Science 332: 1193–1196.

18. WiserMJ, RibeckN, LenskiRE (2013) Long-Term Dynamics of Adaptation in Asexual Populations. Science 342: 1364–1367.

19. FriesenML, SaxerG, TravisanoM, DoebeliM (2004) Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution 58: 245–260.

20. SpencerCC, SaxerG, TravisanoM, DoebeliM (2007) Seasonal resource oscillations maintain diversity in bacterial microcosms. Evolutionary Ecology Research 9: 775–787.

21. HellingRB, VargasCN, AdamsJ (1987) Evolution of Escherichia coli during growth in a constant environment. Genetics 116: 349–358.

22. RosenzweigRF, SharpRR, TrevesDS, AdamsJ (1994) Microbial evolution in a simple unstructured environment: Genetic differentiation in Escherichia coli. Genetics 137: 903–917.

23. StewartFM, LevinBR (1973) Partitioning of resources and outcome of interspecific competition: Model and some general considerations. American Naturalist 107: 171–198.

24. HabetsMGJL, RozenDE, HoekstraRF, de VisserJAGM (2006) The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments. Ecology Letters 9: 1041–1048.

25. RozenDE, LenskiRE (2000) Long-term experimental evolution in Escherichia coli VIII: Dynamics of a balanced polymorphism. American Naturalist 155: 24–35.

26. RaineyPB, TravisanoM (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69–72.

27. RundleHD, NagelL, BoughmanJW, SchluterD (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308.

28. LososJB, JackmanTR, LarsonA, de QueirozK, Rodriguez-SchettinoL (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115–2118.

29. BattestiA, MajdalaniN, GottesmanS (2011) The RpoS-Mediated General Stress Response in Escherichia coli. Annual Review of Microbiology Vol 65 65: 189–213.

30. Notley-McRobbL, SeetoS, FerenciT (2003) The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proceedings of the Royal Society B-Biological Sciences 270: 843–848.

31. BlankD, WolfL, AckermannM, SilanderOK (2014) The predictability of molecular evolution during functional innovation. Proc Natl Acad Sci U S A 111: 3044–3049.

32. MaharjanR, SeetoS, Notley-McRobbL, FerenciT (2006) Clonal adaptive radiation in a constant environment. Science 313: 514–517.

33. EydallinG, RyallB, MaharjanR, FerenciT (2013) The nature of laboratory domestication chagnes in freshly isolated Escherichia coli strains. Environmental Microbiology 16: 611–905.

34. FerenciT (2005) Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Molecular Microbiology 57: 1–8.

35. BjedovI, TenaillonO, GerardB, SouzaV, DenamurE, et al. (2003) Stress-induced mutagenesis in bacteria. Science 300: 1404–1409.

36. Al MamunAM, LombardoMJ, SheeC, LisewskiAM, GonzalezC, et al. (2012) Identity and Function of a Large Gene Network Underlying Mutagenic Repair of DNA Breaks. Science 338: 1344–1348.

37. FinkelSE (2006) Long-term survival during stationary phase: evolution and the GASP phenotype. Nature Reviews Microbiology 4: 113–120.

38. SnyderE, GordonDM, StoebelDM (2012) Escherichia coli Lacking RpoS Are Rare in Natural Populations of Non-Pathogens. G3-Genes Genomes Genetics 2: 1341–1344.

39. KingT, IshihamaA, KoriA, FerenciT (2004) A regulatory trade-off as a source of strain variation in the species Escherichia coli. Journal of Bacteriology 186: 5614–5620.

40. Puentes-TellezPE, HansenMA, SorensenSJ, van ElsasJD (2013) Adaptation and heterogeneity of Escherichia coli MC1000 growing in complex environments. Applied and environmental microbiology 79: 1008–1017.

41. Maltby R, Leatham-Jensen MP, Gibson T, Cohen PS, Conway T (2013) Nutritional Basis for Colonization Resistance by Human Commensal Escherichia coli Strains HS and Nissle 1917 against E. coli O157:H7 in the Mouse Intestine. Plos One 8.

42. ToppingDL, CliftonPM (2001) Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiological Reviews 81: 1031–1064.

43. LynchM (2010) Evolution of the mutation rate. Trends in Genetics 26: 345–352.

44. Saxer G, Havlak P, Fox SA, Quance MA, Gupta S, et al. (2012) Whole Genome Sequencing of Mutation Accumulation Lines Reveals a Low Mutation Rate in the Social Amoeba Dictyostelium discoideum. Plos One 7.

45. Halligan DL, Keightley PD (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annual Review of Ecology Evolution and Systematics 40.

46. PlotkinJB, KudlaG (2011) Synonymous but not the same: the causes and consequences of codon bias. Nature Reviews Genetics 12: 32–42.

47. AnderssonSGE, KurlandCG (1990) Codon Preferences in Free-Living Microorganisms. Microbiological Reviews 54: 198–210.

48. Hengge-Aronis R (2002) Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol Mol Biol Rev 66: : 373–395, table of contents.

49. ParkDM, AkhtarMS, AnsariAZ, LandickR, KileyPJ (2013) The bacterial response regulator ArcA uses a diverse binding site architecture to regulate carbon oxidation globally. PLoS Genet 9: e1003839.

50. Shimizu K (2013) Metabolic Regulation of a Bacterial Cell System with Emphasis on Escherichia coli Metabolism. ISRN Biochemistry 2013.

51. LevanonSS, SanKY, BennettGN (2005) Effect of oxygen on the Escherichia coli ArcA and FNR regulation systems and metabolic responses. Biotechnology and Bioengineering 89: 556–564.

52. Herron MD, Doebeli M (2013) Parallel Evolutionary Dynamics of Adaptive Diversification in Escherichia coli. PloS Biology 11.

53. CooperTF, RozenDE, LenskiRE (2003) Parallel changes in qene expression after 20,000 generations of evolution in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 100: 1072–1077.

54. PerrenoudA, SauerU (2005) Impact of global transcriptional regulation by ArcA, ArcB, Cra, Crp, Cya, Fnr, and Mlc on glucose catabolism in Escherichia coli. Journal of Bacteriology 187: 3171–3179.

55. AmaralL, MartinsA, SpenglerG, MolnarJ (2014) Efflux pumps of Gram-negative bacteria: what they do, how they do it, with what and how to deal with them. Front Pharmacol 4: 168.

56. TaborCW, TaborH (1985) Polyamines in microorganisms. Microbiol Rev 49: 81–99.

57. IuchiS, LinEC (1992) Purification and phosphorylation of the Arc regulatory components of Escherichia coli. J Bacteriol 174: 5617–5623.

58. GeorgellisD, KwonO, De WulfP, LinEC (1998) Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J Biol Chem 273: 32864–32869.

59. Toro-RomanA, MackTR, StockAM (2005) Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: A symmetric dimer mediated by the alpha 4-beta 5-alpha 5 face. Journal of Molecular Biology 349: 11–26.

60. PhilippeN, CrozatE, LenskiRE, SchneiderD (2007) Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29: 846–860.

61. PlucainJ, HindreT, Le GacM, TenaillonO, CruveillerS, et al. (2014) Epistasis and allele specificity in the emergence of a stable polymorphism in Escherichia coli. Science 343: 1366–1369.

62. Puentes-TellezPE, KovacsAT, KuipersOP, van ElsasJD (2014) Comparative genomics and transcriptomics analysis of experimentally evolved Escherichia coli MC1000 in complex environments. Environmental Microbiology 16: 856–870.

63. Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, et al. (1996) Escherichia coli and Salmonella: Cellular and Molecular Biology. Washington, D.C.: ASM Press.

64. BaevMV, BaevD, RadekAJ, CampbellJW (2006) Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of sugars, alcohols, and organic acids with transcriptional microarrays. Applied microbiology and biotechnology 71: 310–316.

65. BaevMV, BaevD, RadekAJ, CampbellJW (2006) Growth of Escherichia coli MG1655 on LB medium: monitoring utilization of amino acids, peptides, and nucleotides with transcriptional microarrays. Applied microbiology and biotechnology 71: 317–322.

66. RahmanM, HasanMR, ObaT, ShimizuK (2006) Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations. Biotechnol Bioeng 94: 585–595.

67. BuchJK, BoyleSM (1985) Biosynthetic arginine decarboxylase in Escherichia coli is synthesized as a precursor and located in the cell envelope. J Bacteriol 163: 522–527.

68. TkachenkoAG, NesterovaL (2001) The role of putrescine in of oxidative stress defense genes expression regulation in Escherichia coli. Mikrobiologiia 70: 168–173.

69. ChattopadhyayMK, TaborCW, TaborH (2009) Polyamines Are Not Required for Aerobic Growth of Escherichia coli: Preparation of a Strain with Deletions in All of the Genes for Polyamine Biosynthesis. Journal of Bacteriology 191: 5549–5552.

70. SchneiderBL, HernandezVJ, ReitzerL (2013) Putrescine catabolism is a metabolic response to several stresses in Escherichia coli. Mol Microbiol 88: 537–550.

71. SturgillG, RatherPN (2004) Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol Microbiol 51: 437–446.

72. BernierSP, LetoffeS, DelepierreM, GhigoJM (2011) Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol Microbiol 81: 705–716.

73. ReitzerL (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annual Review of Microbiology 57: 155–176.

74. WalkiewiczK, CardenasASB, SunC, BacornC, SaxerG, et al. (2012) Small changes in enzyme function can lead to surprisingly large fitness effects during adaptive evolution of antibiotic resistance. Proceedings of the National Academy of Sciences of the United States of America 109: 21408–21413.

75. Pena MI, Davlieva M, Bennett MR, Olson JS, Shamoo Y (2010) Evolutionary fates within a microbial population highlight an essential role for protein folding during natural selection. Molecular Systems Biology 6.

76. Quance MA, Travisano M (2009) Effects of temperature on the fitness cost of resistance to bacteriophage T4 in Escherichia coli. Evolution.

77. KniesJL, IzemR, SuplerKL, KingsolverJG, BurchCL (2006) The genetic basis of thermal reaction norm evolution in lab and natural phage populations. Plos Biology 4: 1257–1264.

78. DongT, SchellhornHE (2010) Role of RpoS in Virulence of Pathogens. Infection and Immunity 78: 887–897.

79. SenguptaN, PaulK, ChowdhuryR (2003) The global regulator arcA modulates expression of virulence factors in Vibrio cholerae. Infection and Immunity 71: 5583–5589.

80. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST server: Rapid annotations using subsystems technology. Bmc Genomics 9.

81. OverbeekR, DiszT, StevensR (2004) The SEED: A peer-to-peer environment for genome annotation. Communications of the Acm 47: 46–51.

82. DeatherageDE, BarrickJE (2014) Identification of Mutations in Laboratory-Evolved Microbes from Next-Generation Sequencing Data Using breseq. Methods Mol Biol 1151: 165–188.

83. RossMG, RussC, CostelloM, HollingerA, LennonNJ, et al. (2013) Characterizing and measuring bias in sequence data. Genome Biol 14: R51.

84. LangGI, RiceDP, HickmanMJ, SodergrenE, WeinstockGM, et al. (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571–574.

85. Whitlock MC, Schluter D (2009) The analysis of biological data. Greenwood Village, CO: Roberts and Company Publishers.

86. ZimmerJS, MonroeME, QianWJ, SmithRD (2006) Advances in proteomics data analysis and display using an accurate mass and time tag approach. Mass Spectrom Rev 25: 450–482.

87. PolpitiyaAD, QianWJ, JaitlyN, PetyukVA, AdkinsJN, et al. (2008) DAnTE: a statistical tool for quantitative analysis of -omics data. Bioinformatics 24: 1556–1558.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 12
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#