Rapid Evolution of Recombinant for Xylose Fermentation through Formation of Extra-chromosomal Circular DNA

English version České info

Xylose is an important component of lignocellulose hydrolysates used for the production of bioethanol, but the yeast Saccharomyces cerevisiae is unable to utilize xylose. Insertion of a bacterial xylose isomerase gene and improvement of growth on xylose by evolutionary adaptation resulted in amplification of this gene and efficient xylose fermentation capacity. Further analysis of the final and intermediate strains from the evolutionary adaptation process revealed interesting features about the mechanisms involved in gene amplification events, which have occurred frequently in natural evolution. We now show that a circular DNA element was spontaneously created by the yeast, encompassing the xylose isomerase gene and an ARS element, present by coincidence adjacent of the inserted xylose isomerase gene. ARS elements are the sites where DNA polymerase initiates duplication of DNA. Interestingly, this has revealed for the first time in yeast that circular DNA plasmids can be created from genomic DNA in the absence of flanking repetitive sequences.

Vyšlo v časopise: Rapid Evolution of Recombinant for Xylose Fermentation through Formation of Extra-chromosomal Circular DNA. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005010
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005010

Souhrn

Zdroje

1. Barrick JE, Lenski RE (2009) Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 74: 119–129. doi: 10.1101/sqb.2009.74.018 19776167

2. Frank SA (2013) Microbial evolution: regulatory design prevents cancer-like overgrowths. Curr Biol 23: R343–346. doi: 10.1016/j.cub.2013.03.046 23660352

3. Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73: 129–169. 11816810

4. Cakar ZP, Turanli-Yildiz B, Alkim C, Yilmaz U (2012) Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res 12: 171–182. doi: 10.1111/j.1567-1364.2011.00775.x 22136139

5. Elena SF, Lenski RE (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457–469. 12776215

6. Katju V, Bergthorsson U (2013) Copy-number changes in evolution: rates, fitness effects and adaptive significance. Front Genet 4: 273. doi: 10.3389/fgene.2013.00273 24368910

7. Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci 279: 5048–5057. doi: 10.1098/rspb.2012.1108 22977152

8. Ames RM, Rash BM, Hentges KE, Robertson DL, Delneri D, et al. (2010) Gene duplication and environmental adaptation within yeast populations. Genome Biol Evol 2: 591–601. doi: 10.1093/gbe/evq043 20660110

9. Despons L, Baret PV, Frangeul L, Louis VL, Durrens P, et al. (2010) Genome-wide computational prediction of tandem gene arrays: application in yeasts. BMC Genomics 11: 56. doi: 10.1186/1471-2164-11-56 20092627

10. Cohen S, Segal D (2009) Extrachromosomal circular DNA in eukaryotes: possible involvement in the plasticity of tandem repeats. Cytogenet Genome Res 124: 327–338. doi: 10.1159/000218136 19556784

11. Gresham D, Usaite R, Germann SM, Lisby M, Botstein D, et al. (2010) Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proc Natl Acad Sci U S A 107: 18551–18556. doi: 10.1073/pnas.1014023107 20937885

12. van Loon N, Miller D, Murnane JP (1994) Formation of extrachromosomal circular DNA in HeLa cells by nonhomologous recombination. Nucleic Acids Res 22: 2447–2452. 8041604

13. Lau MW, Gunawan C, Balan V, Dale BE (2010) Comparing the fermentation performance of Escherichia coli KO11, Saccharomyces cerevisiae 424A(LNH-ST) and Zymomonas mobilis AX101 for cellulosic ethanol production. Biotechnol Biofuels 3: 11. doi: 10.1186/1754-6834-3-11 20507563

14. Olsson L, Linden T, Hahn-Hägerdal B (1992) Performance of microorganisms in spent sulfite liquor and enzymatic hydrolysate of steam-pretreated salix. Appl Biochem Biotech 34–35: 359–368.

15. de Souza AP, Leite DCC, Pattathil S, Hahn MG, Buckeridge MS (2013) Composition and structure of sugarcane cell wall polysaccharides: implications for second-generation bioethanol production. BioEnergy Res 6: 564–579.

16. Limayem A, Ricke SC (2012) Lignocellulosic biomass for bioethanol production: current perspectives, potential issues and future prospects. Prog Energ Combust 38: 449–467.

17. Alper H, Stephanopoulos G (2009) Engineering for biofuels: exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Microbiol 7: 715–723. doi: 10.1038/nrmicro2186 19756010

18. Brat D, Boles E, Wiedemann B (2009) Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl Environ Microbiol 75: 2304–2311. doi: 10.1128/AEM.02522-08 19218403

19. Demeke MM, Dietz H, Li Y, Foulquie-Moreno MR, Mutturi S, et al. (2013) Development of a D-xylose fermenting and inhibitor tolerant industrial Saccharomyces cerevisiae strain with high performance in lignocellulose hydrolysates using metabolic and evolutionary engineering. Biotechnol Biofuels 6: 89. doi: 10.1186/1754-6834-6-89 23800147

20. Araya CL, Payen C, Dunham MJ, Fields S (2010) Whole-genome sequencing of a laboratory-evolved yeast strain. BMC Genomics 11: 88. doi: 10.1186/1471-2164-11-88 20128923

21. Petes TD (1980) Molecular genetics of yeast. Annu Rev Biochem 49: 845–876. 6996573

22. Michel AH, Kornmann B, Dubrana K, Shore D (2005) Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev 19: 1199–1210. 15905408

23. Singh MV, Weil PA (2002) A method for plasmid purification directly from yeast. Anal Biochem 307: 13–17. 12137773

24. Nieduszynski CA, Knox Y, Donaldson AD (2006) Genome-wide identification of replication origins in yeast by comparative genomics. Genes Dev 20: 1874–1879. 16847347

25. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, et al. (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39: 1256–1260. 17828263

26. Carginale V, Trinchella F, Capasso C, Scudiero R, Parisi E (2004) Gene amplification and cold adaptation of pepsin in Antarctic fish. A possible strategy for food digestion at low temperature. Gene 336: 195–205. 15246531

27. Carreto L, Eiriz MF, Gomes AC, Pereira PM, Schuller D, et al. (2008) Comparative genomics of wild type yeast strains unveils important genome diversity. BMC Genomics 9: 524. doi: 10.1186/1471-2164-9-524 18983662

28. Liti G, Louis EJ (2005) Yeast evolution and comparative genomics. Annu Rev Microbiol 59: 135–153. 15877535

29. Kao KC, Sherlock G (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 40: 1499–1504. doi: 10.1038/ng.280 19029899

30. Zhou H, Cheng JS, Wang BL, Fink GR, Stephanopoulos G (2012) Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae. Metab Eng 14: 611–622. doi: 10.1016/j.ymben.2012.07.011 22921355

31. Brown CJ, Todd KM, Rosenzweig RF (1998) Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol Biol Evol 15: 931–942. 9718721

32. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 99: 16144–16149. 12446845

33. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, et al. (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 4: e1000303. doi: 10.1371/journal.pgen.1000303 19079573

34. Payen C, Di Rienzi SC, Ong GT, Pogachar JL, Sanchez JC, et al. (2014) The dynamics of diverse segmental amplifications in populations of Saccharomyces cerevisiae adapting to strong selection. G3 (Bethesda) 4: 399–409. doi: 10.1534/g3.113.009365 24368781

35. Galeote V, Bigey F, Beyne E, Novo M, Legras JL, et al. (2011) Amplification of a Zygosaccharomyces bailii DNA segment in wine yeast genomes by extrachromosomal circular DNA formation. PLoS One 6: e17872. doi: 10.1371/journal.pone.0017872 21423766

36. Hastings PJ, Ira G, Lupski JR (2009) A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet 5: e1000327. doi: 10.1371/journal.pgen.1000327 19180184

37. Hastings PJ, Lupski JR, Rosenberg SM, Ira G (2009) Mechanisms of change in gene copy number. Nat Rev Genet 10: 551–564. doi: 10.1038/nrg2593 19597530

38. Fogel S, Welch JW (1982) Tandem gene amplification mediates copper resistance in yeast. Proc Natl Acad Sci U S A 79: 5342–5346. 6291039

39. Cherest H, Davidian JC, Thomas D, Benes V, Ansorge W, et al. (1997) Molecular characterization of two high affinity sulfate transporters in Saccharomyces cerevisiae. Genetics 145: 627–635. 9055073

40. Gietz RD, Schiestl RH, Willems AR, Woods RA (1995) Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355–360. 7785336

41. Thompson JR, Register E, Curotto J, Kurtz M, Kelly R (1998) An improved protocol for the preparation of yeast cells for transformation by electroporation. Yeast 14: 565–571. 9605506

42. Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267–272. 3319781

43. Johnston JR (1994) Molecular genetics of yeast: A practical approach. New York: Oxford University Press.