Evolutionary engineering and transcriptomic analysis of nickel-resistant Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 13, Issue 8, 2013, Pages 731-746

  Küçükgöze, Gökhan ^a   Alkim, Ceren ^a   Yilmaz, Ülkü ^a   Kisakesen, H Ibrahim ^a,b   Gündüz, Sema ^a   Akman, Süleyman ^a   Çakar, Z Petek ^a  

^a ISTANBUL TECHNICAL UNIVERSITY   (Turkey)

^b SEM Lab A   (Turkey)

Author keywords

Evolutionary engineering; Inverse metabolic engineering; Nickel resistance; Saccharomyces cerevisiae; Stress resistance; Yeast DNA microarray analysis

Indexed keywords

COBALT; IRON; MANGANESE; NICKEL; ZINC;

ARTICLE; BIOACCUMULATION; BIOENGINEERING; CHEMICAL STRESS; CONTROLLED STUDY; CROSS RESISTANCE; EVOLUTIONARY ENGINEERING; FUNGAL GENE; FUNGUS MUTANT; HOMEOSTASIS; NICKEL RESISTANCE; NONHUMAN; OXIDATIVE STRESS; PHYSICAL RESISTANCE; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOMICS; UPREGULATION;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EVOLUTIONARY ENGINEERING; INVERSE METABOLIC ENGINEERING; NICKEL RESISTANCE; SACCHAROMYCES CEREVISIAE; STRESS RESISTANCE; YEAST DNA MICROARRAY ANALYSIS;

CARBOHYDRATES; DRUG RESISTANCE, FUNGAL; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; MUTATION; NICKEL; PHENOTYPE; SACCHAROMYCES CEREVISIAE; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84887608790     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/1567-1364.12073     Document Type: Article

References (55)

1. Alkim C, Benbadis L, Yilmaz U, Cakar ZP & Francois JM (2013) Mechanisms other than activation of the iron regulon account for the hyper-resistance to cobalt of a Saccharomyces cerevisiae strain obtained by evolutionary engineering. Metallomics 5: 1043-1060. DOI: 10.1039/C3MT00107E.
2. Arita A, Zhou X, Ellen TP et al. (2009) A genome-wide deletion mutant screen identifies pathways affected by nickel sulfate in Saccharomyces cerevisiae. BMC Genomics 10: 524.
3. Askwith C, Eide D, Van Ho A, Bernard PS, Li L, Davis-Kaplan S, Sipe DM & Kaplan J (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76: 403-410.
4. Bell PJL (2004) Yeast differentiation using histone promoter sequences. Lett Appl Microbiol 38: 388-392.
5. Benjamini Y & Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
6. Bissinger PH, Wieser R, Hamilton B & Ruis H (1989) Control of Saccharomyces cerevisiae catalase T gene (CTT1) expression by nutrient supply via the RAS-cyclic AMP pathway. Mol Cell Biol 9: 1309-1315.
7. Blaisseau PL, Lesuisse E & Camadro JM (2001) Aft2p, a novel iron-regulated transcription activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast. J Biol Chem 276: 34221-34226.
8. Bleackley MR, Young BP, Loewen CJR & MacGillivray RTA (2011) High density array screening to identify the genetic requirements for transition metal tolerance in Saccharomyces cerevisiae. Metallomics 3: 195-205.
9. Butler PR, Brown M & Oliver SG (1996) Improvement of antibiotic titers from Streptomyces bacteria by interactive continuous selection. Biotechnol Bioeng 49: 185-196.
10. Çakar ZP, Seker UO, Tamerler C, Sonderegger M & Sauer U (2005) Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res 5: 569-578.
11. Çakar ZP, Alkim C, Turanli B, Tokman N, Akman S, Sarikaya M, Tamerler C, Benbadis L & Francois JM (2009) Isolation of cobalt hyper-resistant mutants of Saccharomyces cerevisiae by in vivo evolutionary engineering approach. J Biotechnol 143: 130-138.
12. Çakar ZP, Turanli-Yildiz B, Alkim C & Yilmaz Ü (2012) Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties. FEMS Yeast Res 12: 171-182.
13. Cempel M & Nikel G (2006) Nickel: a review of its sources and environmental toxicology. Pol J Environ Stud 15: 375-382.
14. Conklin DS, Culbertson MR & Kung C (1994) Interactions between gene products involved in divalent cation transport in Saccharomyces cerevisiae. Mol Gen Genet 244: 303-311.
15. Cramp DG (1967) New automated method for measuring glucose by glucose oxidase. J Clin Pathol 20: 910-912.
16. De Silva DM, Askwith CC, Eide D & Kaplan J (1995) The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J Biol Chem 270: 1098-1101.
17. Denkhaus E & Salnikow K (2002) Nickel essentiality toxicity and carcinogenicity. Crit Rev Oncol Hematol 42: 35-56.
18. Eide DJ, Clark S, Nair TM, Gehl M, Gribskov M, Guerinot ML & Harper JF (2005) Characterization of the yeast ionome: a genome-wide analysis of nutrient mineral and trace element homeostasis in Saccharomyces cerevisiae. Genome Biol 6: R77.
19. Eitinger T & Mandrand-Berthelot MA (2000) Nickel transport systems in microorganisms. Arch Microbiol 173: 1-9.
20. Eitinger T, Degen O, Bohnke U & Muller M (2000) Nic1p a relative of bacterial transition metal permeases in Schizosaccharomyces pombe provides nickel ion for urease biosynthesis. J Biol Chem 275: 33184.
21. Entian KD & Kötter P (2007) Yeast genetic strain and plasmid collections. Methods Microbiol 36: 629-666.
22. +2 in Saccharomyces cerevisiae cells. Biosci Biotechnol Biochem 69: 2343-2348.
23. François J & Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 25: 125-145.
24. Guimaraes PM, Francois J, Parrou JL, Teixeira JA & Domingues L (2008) Adaptive evolution of a lactose-consuming Saccharomyces cerevisiae recombinant. Appl Environ Microbiol 74: 1748-1756.
25. Haugen AC, Kelley R, Collins JB, Tucker CJ, Deng C, Afshari CA, Brown JM, Ideker T & Van Houten B (2004) Integrating phenotypic and expression profiles to map arsenic-response networks. Genome Biol 5: R95.
26. Jin YH, Dunlap PE, McBride SJ, Al-Refai H, Bushel PR & Freedman JH (2008) Global transcriptome and deletome profiles of yeast exposed to transition metals. PLoS Genet 4: e1000053, DOI:10.1371/journal.pgen.1000053.
27. +2. Microbios 67: 177-186.
28. Joho M, Ishikawa Y, Kunikane M, Inouhe M, Tohoyama H & Murayama T (1992) The subcellular distribution of nickel ion in Ni-sensitive and Ni-resistant strains of Saccharomyces cerevisiae. Microbios 71: 149-159.
29. Joho M, Inouhe M, Tohoyama H & Murayama T (1995) Nickel ion resistance mechanisms in yeasts and other fungi. J Ind Microbiol 14: 164-168.
30. Kasprzak KS, Sunderman FW Jr & Salnikow K (2003) Nickel carcinogenesis. Mutat Res 533: 67-97.
31. Lawrence CW (1991) Classical mutagenesis techniques. Methods Enzymol 194: 456-464.
32. Li L, Chen OS, McVey Ward D & Kaplan J (2001) CCC1 is a transporter that mediates vacuolar iron storage in yeast. J Biol Chem 276: 29515-29519.
33. Minty JJ, Lesnefsky AA, Lin F et al. (2011) Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli. Microb Cell Fact 10: 18.
34. Mulrooney SB & Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27: 239-261.
35. Nevoigt E (2008) Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 72: 379-412.
36. Nishimura K, Igarashi K & Kakinuma Y (1998) Proton gradient-driven nickel uptake by vacuolar membrane vesicles of Saccharomyces cerevisiae. J Bacteriol 180: 1962-1965.
37. Parrou JL & François J (1997) A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal Biochem 248: 186-193.
38. Philpott CC & Protchenko O (2008) Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot Cell 7: 20-27.
39. Puig S, Askeland E & Thiele DJ (2005) Coordinated remodeling of cellular metabolism during iron deficiency through targeted mRNA degradation. Cell 120: 99-110.
40. Reck BK, Müller DB, Rostkowski K & Graedel TE (2008) Anthropogenic nickel cycle: insights into use trade and recycling. Environ Sci Technol 42: 3394-3400.
41. Robinson MD, Grigull J, Mohammad N & Hughes TR (2002) FunSpec: a web-based cluster interpreter for yeast. BMC Bioinformatics 3: 35.
42. Ruepp A, Zollner A, Maier D et al. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32: 5539-5545.
43. Ruotolo R, Marchini G & Ottonello S (2008) Membrane transporters and protein traffic networks differentially affecting metal tolerance: a genomic phenotyping study in yeast. Genome Biol 9: R67.
44. Russek E & Colwell RR (1983) Computation of most probable numbers. Appl Environ Microbiol 45: 1646-1650.
45. Rutherford JC, Ojeda L, Balk J, Mühlenhoff U, Lill R & Winge DR (2005) Activation of the iron regulon by the yeast Aft1/Aft2 transcription factors depends on mitochondrial but not cytosolic iron-sulfur protein biogenesis. J Biol Chem 280: 10135-11040.
46. Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73: 130-166.
47. T method. Nat Protoc 3: 1101-1108.
48. Şen M, Yilmaz Ü, Baysal A, Akman S & Çakar ZP (2011) In vivo evolutionary engineering of a boron-resistant bacterium: Bacillus boroniphilus. Antonie Van Leeuwenhoek 99: 825-835.
49. Stadler JA & Schweyen RJ (2002) The yeast iron regulon is induced upon cobalt stress and crucial for cobalt tolerance. J Biol Chem 277: 39649-39654.
50. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD & Dancis A (1996) A permease-oxidase complex involved in high affinity iron uptake in yeast. Science 271: 1552-1557.
51. Takumi S, Kimura H, Matsusaki H, Kawazoe S, Tominaga N & Arizono K (2010) DNA microarray analysis of genomic responses of yeast Saccharomyces cerevisiae to nickel chloride. J Toxicol Sci 35: 125-129.
52. Valko M, Morris H & Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12: 1161-1208.
53. Wisselink HW, Toirkens MJ, Wu Q, Pronk JT & van Maris AJ (2009) Novel evolutionary engineering approach for accelerated utilization of glucose xylose and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 75: 907-914.
54. Yamaguchi-Iwai Y, Dancis A & Klausner RD (1995) AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J 4: 1231-1239.
55. Yasokawa D & Iwahashi H (2010) Toxicogenomics using yeast DNA microarrays. J Biosci Bioeng 110: 511-522.