Phenotypic innovation through recombination in genome-scale metabolic networks

Proceedings of the Royal Society B: Biological Sciences

Volumn 283, Issue 1839, 2016, Pages

  Hosseini, Sayed Rzgar ^a,b   Martin, Olivier C ^c   Wagner, Andreas ^a,b,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c INRA Institut National de la Recherche Agronomique   (France)

^d SANTA FE INSTITUTE   (United States)

Author keywords

Genome scale metabolic networks; Metabolic genotype; Metabolic innovation; Metabolic phenotype; Recombination; Superessential reactions

Indexed keywords

BIOCHEMISTRY; EXPERIMENTAL STUDY; GENOME; GENOTYPE; METABOLISM; PHENOTYPE; PHYSIOLOGICAL RESPONSE; PROKARYOTE; RECOMBINATION; SURVIVAL;

PROKARYOTA;

EID: 84989329128     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2016.1536     Document Type: Article

References (66)

1. Smith JM. 1978 The evolution of sex. Cambridge, UK: Cambridge University Press.
2. Otto SP, Lenormand T. 2002 Resolving the paradox of sex and recombination. Nat. Rev. Genet. 3, 252-261.(doi:10.1038/nrg761)
3. Hartfield M, Keightley PD. 2012 Current hypotheses for the evolution of sex and recombination. Integr. Zool. 7, 192-209.(doi:10.1111/j.1749-4877.2012.00284.x)
4. Fisher RA. 1930 The genetical theory of natural selection: a complete variorum edition. Oxford, UK: Oxford University Press.
5. Muller HJ. 1932 Some genetic aspects of sex. Am. Nat. 66, 118-138.(doi:10.1086/280418)
6. Keightley PD, Otto SP. 2006 Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443, 89-92.(doi:10.1038/nature05049)
7. Stemmer WP. 1994 DNA shuffling by random fragmentation and reassembly: in vitro recombination for molecular evolution. Proc. Natl Acad. Sci. USA 91, 10 747-10 751.(doi:10.1073/pnas.91.22.10747)
8. Zhang Y-X, Perry K, Vinci VA, Powell K, Stemmer WPC, del Cardayré SB. 2002 Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature 415, 644-646.(doi:10.1038/415644a)
9. Crameri A, Dawes G, Rodriguez E, Silver S, Stemmer WP. 1997 Molecular evolution of an arsenate detoxification pathway by DNA shuffling. Nat. Biotechnol. 15, 436-438.(doi:10.1038/nbt0597-436)
10. Chang CC, Chen TT, Cox BW, Dawes GN, Stemmer WP, Punnonen J, Patten PA. 1999 Evolution of a cytokine using DNA family shuffling. Nat. Biotechnol. 17, 793-797.(doi:10.1038/70147)
11. Ness JE, Welch M, Giver L, Bueno M, Cherry JR, Borchert TV, Stemmer WP, Minshull J. 1999 DNA shuffling of subgenomic sequences of subtilisin. Nat. Biotechnol. 17, 893-896.(doi:10.1038/12884)
12. Martin OC, Wagner A. 2009 Effects of recombination on complex regulatory circuits. Genetics 183, 673-684, 1SI-8SI.(doi:10.1534/genetics.109.104174)
13. Cui Y, Wong WH, Bornberg-Bauer E, Chan HS. 2002 Recombinatoric exploration of novel folded structures: a heteropolymer-based model of protein evolutionary landscapes. Proc. Natl Acad. Sci. USA 99, 809-814.(doi:10.1073/pnas.022240299)
14. Drummond DA, Silberg JJ, Meyer MM, Wilke CO, Arnold FH. 2005 On the conservative nature of intragenic recombination. Proc. Natl Acad. Sci. USA 102, 5380-5385.(doi:10.1073/pnas.0500729102)
15. Feist AM, Palsson BØ. 2008 The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli. Nat. Biotechnol. 26, 659-667.(doi:10.1038/nbt1401)
16. McCloskey D, Palsson BØ, Feist AM. 2013 Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli. Mol. Syst. Biol. 9, 661.(doi:10.1038/msb.2013.18)
17. Lewis NE, Nagarajan H, Palsson BO. 2012 Constraining the metabolic genotype-phenotype relationship using a phylogeny of in silico methods. Nat. Rev. Microbiol. 10, 291-305.(doi:10.1038/nrmicro2737)
18. Matias Rodrigues JF, Wagner A. 2009 Evolutionary plasticity and innovations in complex metabolic reaction networks. PLoS Comput. Biol. 5, e1000613.(doi:10.1371/journal.pcbi.1000613)
19. Orth JD, Thiele I, Palsson BØ. 2010 What is flux balance analysis? Nat. Biotechnol. 28, 245-248.(doi:10.1038/nbt.1614)
20. Edwards JS, Ibarra RU, Palsson BO. 2001 In silico predictions of Escherichia coli metabolic capabilities are consistent with experimental data. Nat. Biotechnol. 19, 125-130.(doi:10.1038/84379)
21. Edwards JS, Palsson BO. 2000 The Escherichia coli MG1655 in silico metabolic genotype: its definition, characteristics, and capabilities. Proc. Natl Acad. Sci. USA 97, 5528-5533.(doi:10.1073/pnas.97.10.5528)
22. Edwards JS, Palsson BO. 1999 Systems properties of the Haemophilus influenzae Rd metabolic genotype. J. Biol. Chem. 274, 17 410-17 416.(doi:10.1074/jbc.274.25.17410)
23. Samal A, Matias Rodrigues JF, Jost J, Martin OC, Wagner A. 2010 Genotype networks in metabolic reaction spaces. BMC Syst. Biol. 4, 30.(doi:10.1186/1752-0509-4-30)
24. Barve A, Hosseini S-R, Martin OC, Wagner A. 2014 Historical contingency and the gradual evolution of metabolic properties in central carbon and genomescale metabolisms. BMC Syst. Biol. 8, 48.(doi:10.1186/1752-0509-8-48)
25. Hosseini SR, Barve A, Wagner A. 2015 Exhaustive analysis of a genotype space comprising 1015 central carbon metabolisms reveals an organization conducive to metabolic innovation. PLoS Comput. Biol. 11, e1004329.(doi:10.1371/journal.pcbi.1004329)
26. Copley SD. 2000 Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem. Sci. 25, 261-265.(doi:10.1016/S0968-0004(00)01562-0)
27. Rehmann L, Daugulis AJ. 2008 Enhancement of PCB degradation by Burkholderia xenovorans LB400 in biphasic systems by manipulating culture conditions. Biotechnol. Bioeng. 99, 521-528.(doi:10.1002/bit.21610)
28. Van der Meer JR, Werlen C, Nishino S, Spain J. 1998 Evolution of a pathway for chlorobenzene metabolism leads to natural attenuation in contaminated groundwater. Appl. Environ. Microbiol. 64, 4185-4193.
29. Cline RE, Hill RH, Phillips DL, Needham LL. 1989 Pentachlorophenol measurements in body fluids of people in log homes and workplaces. Arch. Environ. Contam. Toxicol. 18, 475-481.(doi:10.1007/BF01055012)
30. Dantas G, Sommer MOA, Oluwasegun RD, Church GM. 2008 Bacteria subsisting on antibiotics. Science 320, 100-103.(doi:10.1126/science.1155157)
31. Detkova EN, Boltyanskaya YV. 2007 Osmoadaptation of haloalkaliphilic bacteria: role of osmoregulators and their possible practical application. Microbiology 76, 511-522.(doi:10.1134/S0026261707050013)
32. Thomas CM, Nielsen KM. 2005 Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3, 711-721.(doi:10.1038/nrmicro1234)
33. Guttman DS, Dykhuizen DE. 1994 Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266, 1380-1383.(doi:10.1126/science.7973728)
34. Feil EJ et al. 2001 Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc. Natl Acad. Sci. USA 98, 182-187.(doi:10.1073/pnas.98.1.182)
35. Whitaker RJ, Grogan DW, Taylor JW. 2005 Recombination shapes the natural population structure of the hyperthermophilic archaeon Sulfolobus islandicus. Mol. Biol. Evol. 22, 2354-2361.(doi:10.1093/molbev/msi233)
36. Ochman H, Lawrence JG, Groisman EA. 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304.(doi:10.1038/35012500)
37. Pál C, Papp B, Lercher MJ. 2005 Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat. Genet. 37, 1372-1375.(doi:10.1038/ng1686)
38. Fraser C, Hanage WP, Spratt BG. 2007 Recombination and the nature of bacterial speciation. Science 315, 476-480.(doi:10.1126/science.1127573)
39. Majewski J, Zawadzki P, Pickerill P, Cohan FM, Dowson CG. 2000 Barriers to genetic exchange between bacterial species: Streptococcus pneumoniae transformation. J. Bacteriol. 182, 1016-1023.(doi:10.1128/JB.182.4.1016-1023.2000)
40. Kowalczykowski SC, Dixon DA, Eggleston AK, Lauder SD, Rehrauer WM. 1994 Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev. 58, 401-465.
41. Kuo C-H, Ochman H. 2009 The fate of new bacterial genes. FEMS Microbiol. Rev. 33, 38-43.(doi:10.1111/j.1574-6976.2008.00140.x)
42. Mira A, Ochman H, Moran NA. 2001 Deletional bias and the evolution of bacterial genomes. Trends Genet. 17, 589-596.(doi:10.1016/S0168-9525(01)02447-7)
43. Matias Rodrigues JF, Wagner A. 2011 Genotype networks, innovation, and robustness in sulfur metabolism. BMC Syst. Biol. 5, 39.(doi:10.1186/1752-0509-5-39)
44. Wagner A, Andriasyan V, Barve A. 2014 The organization of metabolic genotype space facilitates adaptive evolution in nitrogen metabolism. J. Mol. Biochem. 3, 2-13.(doi:10.5167/uzh-107400)
45. Barve A, Rodrigues JFM, Wagner A. 2012 Superessential reactions in metabolic networks. Proc. Natl Acad. Sci. USA 109, E1121-E1130.(doi:10.1073/pnas.1113065109)
46. Goto S, Nishioka T, Kanehisa M. 2000 LIGAND: chemical database of enzyme reactions. Nucleic Acids Res. 28, 380-382.(doi:10.1093/nar/28.1.380)
47. Kanehisa M, Goto S, Furumichi M, Tanabe M, Hirakawa M. 2010 KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res. 38, D355-D360.(doi:10.1093/nar/gkp896)
48. Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M. 2006 From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res. 34, D354-D357.(doi:10.1093/nar/gkj102)
49. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BØ. 2007 A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3, 121.(doi:10.1038/msb4100155)
50. King ZA, Lu J, Dräger A, Miller P, Federowicz S, Lerman JA, Ebrahim A, Palsson BO, Lewis NE. 2015 BiGG models: a platform for integrating, standardizing and sharing genome-scale models. Nucleic Acids Res. 44, D515-D522.(doi:10.1093/nar/gkv1049)
51. Gelius-Dietrich G, Desouki AA, Fritzemeier CJ, Lercher MJ. 2013 Sybil-efficient constraint-based modelling in R. BMC Syst. Biol. 7, 125.(doi:10.1186/1752-0509-7-125)
52. Tatusova T, Ciufo S, Fedorov B, O’Neill K, Tolstoy I. 2014 RefSeq microbial genomes database: new representation and annotation strategy. Nucleic Acids Res. 42, D553-D559.(doi:10.1093/nar/gkt1274)
53. Trudeau DL, Smith MA, Arnold FH. 2013 Innovation by homologous recombination. Curr. Opin. Chem. Biol. 17, 902-909.(doi:10.1016/j.cbpa.2013.10.007)
54. Apic G, Russell RB. 2010 Domain recombination: a workhorse for evolutionary innovation. Sci. Signal. 3, e30.(doi:10.1126/scisignal.3139pe30)
55. Wagner A. 2012 The role of robustness in phenotypic adaptation and innovation. Proc. R. Soc. B 279, 1249-1258.(doi:10.1098/rspb.2011.2293)
56. Fares MA. 2015 Survival and innovation: the role of mutational robustness in evolution. Biochimie 119, 254-261.(doi:10.1016/j.biochi.2014.10.019)
57. Wagner A. 2011 The molecular origins of evolutionary innovations. Trends Genet. 27, 397-410.(doi:10.1016/j.tig.2011.06.002)
58. Jacob F, Monod J. 1961 Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3, 318-356.(doi:10.1016/S0022-2836(61)80072-7)
59. Itoh T, Takemoto K, Mori H, Gojobori T. 1999 Evolutionary instability of operon structures disclosed by sequence comparisons of complete microbial genomes. Mol. Biol. Evol. 16, 332-346.(doi:10.1093/oxfordjournals.molbev.a026114)
60. Price MN, Arkin AP, Alm EJ. 2006 The life-cycle of operons. PLoS Genet. 2, e96.(doi:10.1371/journal.pgen.0020096)
61. Hunter RL, Markert CL. 1957 Histochemical demonstration of enzymes separated by zone electrophoresis in starch gels. Science 125, 1294-1295.(doi:10.1126/science.125.3261.1294-a)
62. Khersonsky O, Tawfik DS. 2010 Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79, 471-505.(doi:10.1146/annurevbiochem-030409-143718)
63. Kim J, Kershner JP, Novikov Y, Shoemaker RK, Copley SD. 2010 Three serendipitous pathways in E. coli can bypass a block in pyridoxal-50-phosphate synthesis. Mol. Syst. Biol. 6, 436.(doi:10.1038/msb.2010.88)
64. Nam H, Lewis NE, Lerman JA, Lee D-H, Chang RL, Kim D, Palsson BO. 2012 Network context and selection in the evolution to enzyme specificity. Science 337, 1101-1104.(doi:10.1126/science.1216861)
65. Fang G, Rocha EPC, Danchin A. 2008 Persistence drives gene clustering in bacterial genomes. BMC Genomics 9, 4.(doi:10.1186/1471-2164-9-4)
66. Fang G, Rocha E, Danchin A. 2005 How essential are nonessential genes? Mol. Biol. Evol. 22, 2147-2156.(doi:10.1093/molbev/msi211)