Implications of evolutionary engineering for growth and recombinant protein production in methanol-based growth media in the yeast Pichia pastoris

Microbial Cell Factories

Volumn 16, Issue 1, 2017, Pages

  Moser, Josef W ^a,b   Prielhofer, Roland ^a,b   Gerner, Samuel M ^c   Graf, Alexandra B ^b,c   Wilson, Iain B H ^a   Mattanovich, Diethard ^a,b   Dragosits, Martin ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

^c Fachhochschule Campus Wien   (Austria)

Author keywords

Experimental evolution; Methanol; Pichia pastoris; Recombinant protein

Indexed keywords

ALCOHOL OXIDASE; METHANOL; RECOMBINANT PROTEIN; ALCOHOL DEHYDROGENASE; CULTURE MEDIUM;

ARTICLE; BIOENGINEERING; CONTROLLED STUDY; CULTURE MEDIUM; FED BATCH CULTURE; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; GROWTH RATE; KOMAGATAELLA PASTORIS; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; BATCH CELL CULTURE; BIOSYNTHESIS; BIOTECHNOLOGY; CHEMISTRY; DIRECTED MOLECULAR EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR CLONING; MUTATION; PICHIA; PILOT STUDY; PROCEDURES; PROMOTER REGION;

ALCOHOL OXIDOREDUCTASES; BATCH CELL CULTURE TECHNIQUES; BIOTECHNOLOGY; CLONING, MOLECULAR; CULTURE MEDIA; DIRECTED MOLECULAR EVOLUTION; METHANOL; MUTATION; PICHIA; PILOT PROJECTS; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS;

EID: 85015682820     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-017-0661-5     Document Type: Article

References (67)

1. Kurtzman CP. Biotechnological strains of Komagataella (Pichia) pastoris are Komagataella phaffii as determined from multigene sequence analysis. J Ind Microbiol Biotechnol. 2009;36:1435-8.
2. Cregg J, Cereghino J, Shi J, Higgins D. Recombinant protein expression in Pichia pastoris. Mol Biotechnol. 2000;16:23-52.
3. Jacobs P, Geysens S, Vervecken W, Contreras R, Callewaert N. Engineering complex-type N-glycosylation in Pichia pastoris using GlycoSwitch technology. Nat Protoc. 2009;4:58-70.
4. Hamilton S, Gerngross T. Glycosylation engineering in yeast: the advent of fully humanized yeast. Curr Opin Biotechnol. 2007;18:387-92.
5. Baumann K, Carnicer M, Dragosits M, Graf AB, Stadlmann J, Jouhten P, Maaheimo H, Gasser B, Albiol J, Mattanovich D, Ferrer P. A multi-level study of recombinant Pichia pastoris in different oxygen conditions. BMC Syst Biol. 2010;4:141.
6. Dragosits M, Stadlmann J, Graf A, Gasser B, Maurer M, Sauer M, Kreil DP, Altmann F, Mattanovich D. The response to unfolded protein is involved in the osmotolerance of Pichia pastoris. BMC Genom. 2010;11:207.
7. Dragosits M, Stadlmann J, Albiol J, Baumann K, Maurer M, Gasser B, Sauer M, Altmann F, Ferrer P, Mattanovich D. The effect of temperature on the proteome of recombinant Pichia pastoris. J Proteome Res. 2009;8:1380-92.
8. Gasser B, Maurer M, Gach J, Kunert R, Mattanovich D. Engineering of Pichia pastoris for improved production of antibody fragments. Biotechnol Bioeng. 2006;94:353-61.
9. Xu P, Raden D, Doyle FR, Robinson A. Analysis of unfolded protein response during single-chain antibody expression in Saccharomyces cerevisiae reveals different roles for BiP and PDI in folding. Metab Eng. 2005;7:269-79.
10. Gupta P, Ghosalkar A, Mishra S, Chaudhuri T. Enhancement of over expression and chaperone assisted yield of folded recombinant aconitase in Escherichia coli in bioreactor cultures. J Biosci Bioeng. 2009;107:102-7.
11. Waterham H, Digan M, Koutz P, Lair S, Cregg J. Isolation of the Pichia pastoris glyceraldehyde-3-phosphate dehydrogenase gene and regulation and use of its promoter. Gene. 1997;186:37-44.
12. Invitrogen: Pichia expression kit, User manual. 2010.
13. Shen W, Xue Y, Liu Y, Kong C, Wang X, Huang M, Cai M, Zhou X, Zhang Y, Zhou M. A novel methanol-free Pichia pastoris system for recombinant protein expression. Microb Cell Fact. 2016;15:178.
14. Gasser B, Steiger MG, Mattanovich D. Methanol regulated yeast promoters: production vehicles and toolbox for synthetic biology. Microb Cell Fact. 2015;14:196.
15. Krainer FW, Dietzsch C, Hajek T, Herwig C, Spadiut O, Glieder A. Recombinant protein expression in Pichia pastoris strains with an engineered methanol utilization pathway. Microb Cell Fact. 2012;11:22.
16. Kim SJ, Lee JA, Kim YH, Song BK. Optimization of the functional expression of Coprinus cinereus peroxidase in Pichia pastoris by varying the host and promoter. J Microbiol Biotechnol. 2009;19:966-71.
17. Hartner FS, Ruth C, Langenegger D, Johnson SN, Hyka P, Lin-Cereghino GP, Lin-Cereghino J, Kovar K, Cregg JM, Glieder A. Promoter library designed for fine-tuned gene expression in Pichia pastoris. Nucleic Acids Res. 2008;36:e76.
18. Prielhofer R, Cartwright SP, Graf AB, Valli M, Bill RM, Mattanovich D, Gasser B. Pichia pastoris regulates its gene-specific response to different carbon sources at the transcriptional, rather than the translational, level. BMC Genom. 2015;16:167.
19. Rußmayer H, Buchetics M, Gruber C, Valli M, Grillitsch K, Modarres G, Guerrasio R, Klavins K, Neubauer S, Drexler H, et al. Systems-level organization of yeast methylotrophic lifestyle. BMC Biol. 2015;13:80.
20. Wang X, Wang Q, Wang J, Bai P, Shi L, Shen W, Zhou M, Zhou X, Zhang Y, Cai M. Mit1 transcription factor mediates methanol signaling and regulates the alcohol oxidase 1 (AOX1) promoter in Pichia pastoris. J Biol Chem. 2016;291:6245-61.
21. Sahu U, Krishna Rao K, Rangarajan PN. Trm1p, a Zn(II)(2)Cys(6)-type transcription factor, is essential for the transcriptional activation of genes of methanol utilization pathway, in Pichia pastoris. Biochem Biophys Res Commun. 2014;451:158-64.
22. Lin-Cereghino GP, Godfrey L, de la Cruz BJ, Johnson S, Khuongsathiene S, Tolstorukov I, Yan M, Lin-Cereghino J, Veenhuis M, Subramani S, Cregg JM. Mxr1p, a key regulator of the methanol utilization pathway and peroxisomal genes in Pichia pastoris. Mol Cell Biol. 2006;26:883-97.
23. Tenaillon O, Barrick JE, Ribeck N, Deatherage DE, Blanchard JL, Dasgupta A, Wu GC, Wielgoss S, Cruveiller S, Médigue C, et al. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature. 2016;536:165-70.
24. Cooper V, Lenski R. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature. 2000;407:736-9.
25. Hong KK, Nielsen J. Adaptively evolved yeast mutants on galactose show trade-offs in carbon utilization on glucose. Metab Eng. 2013;16:78-86.
26. Conrad TM, Lewis NE, Palsson B. Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol. 2011;7:509.
27. Dragosits M, Mattanovich D. Adaptive laboratory evolution-principles and applications for biotechnology. Microb Cell Fact. 2013;12:64.
28. Dunham MJ. Experimental evolution in yeast: a practical guide. Methods Enzymol. 2010;470:487-507.
29. Notley-McRobb L, King T, Ferenci T. rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol. 2002;184:806-11.
30. Kvitek DJ, Sherlock G. Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet. 2013;9:e1003972.
31. Lee DH, Feist AM, Barrett CL, Palsson B. Cumulative number of cell divisions as a meaningful timescale for adaptive laboratory evolution of Escherichia coli. PLoS ONE. 2011;6:e26172.
32. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. Embnet J. 2011;17:1
33. Chapman JA, Ho I, Sunkara S, Luo S, Schroth GP, Rokhsar DS. Meraculous: de novo genome assembly with short paired-end reads. PLoS ONE. 2011;6:e23501.
34. Küberl A, Schneider J, Thallinger GG, Anderl I, Wibberg D, Hajek T, Jaenicke S, Brinkrolf K, Goesmann A, Szczepanowski R, et al. High-quality genome sequence of Pichia pastoris CBS7435. J Biotechnol. 2011;154:312-20.
35. Galardini M, Biondi EG, Bazzicalupo M, Mengoni A. CONTIGuator: a bacterial genomes finishing tool for structural insights on draft genomes. Source Code Biol Med. 2011;6:11.
36. Stanke M, Morgenstern B. AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res. 2005;33:W465-7.
37. Gardner SN, Slezak T, Hall BG. kSNP3.0: SNP detection and phylogenetic analysis of genomes without genome alignment or reference genome. Bioinformatics. 2015;31:2877-8.
38. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA. The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010;20:1297-303.
39. Nijkamp JF, van den Broek MA, Geertman JM, Reinders MJ, Daran JM, de Ridder D. De novo detection of copy number variation by co-assembly. Bioinformatics. 2012;28:3195-202.
40. Klambauer G, Schwarzbauer K, Mayr A, Clevert DA, Mitterecker A, Bodenhofer U, Hochreiter S. cn.MOPS: mixture of Poissons for discovering copy number variations in next-generation sequencing data with a low false discovery rate. Nucleic Acids Res. 2012;40:e69.
41. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821-9.
42. Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. Integrative genomics viewer. Nat Biotechnol. 2011;29:24-6.
43. Marx H, Sauer M, Resina D, Vai M, Porro D, Valero F, Ferrer P, Mattanovich D. Cloning, disruption and protein secretory phenotype of the GAS1 homologue of Pichia pastoris. FEMS Microbiol Lett. 2006;264:40-7.
44. Dragosits M, Yan S, Razzazi-Fazeli E, Wilson IB, Rendic D. Enzymatic properties and subtle differences in the substrate specificity of phylogenetically distinct invertebrate N-glycan processing hexosaminidases. Glycobiology. 2015;25:448-64.
45. Delic M, Mattanovich D, Gasser B. Repressible promoters-a novel tool to generate conditional mutants in Pichia pastoris. Microb Cell Fact. 2013;12:6.
46. Kobayashi K, Kuwae S, Ohya T, Ohda T, Ohyama M, Ohi H, Tomomitsu K, Ohmura T. High-level expression of recombinant human serum albumin from the methylotrophic yeast Pichia pastoris with minimal protease production and activation. J Biosci Bioeng. 2000;89:55-61.
47. Marx H, Mecklenbräuker A, Gasser B, Sauer M, Mattanovich D. Directed gene copy number amplification in Pichia pastoris by vector integration into the ribosomal DNA locus. FEMS Yeast Res. 2009;9:1260-70.
48. Tenaillon O, Rodríguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, Gaut BS. The molecular diversity of adaptive convergence. Science. 2012;335:457-61.
49. Koch C, Neumann P, Valerius O, Feussner I, Ficner R. Crystal structure of alcohol oxidase from Pichia pastoris. PLoS ONE. 2016;11:e0149846.
50. Smith RL, Johnson AD. Turning genes off by Ssn6-Tup1: a conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci. 2000;25:325-30.
51. Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev. 2002;66:300-72.
52. Avery SV. Microbial cell individuality and the underlying sources of heterogeneity. Nat Rev Microbiol. 2006;4:577-87.
53. Notley-McRobb L, Seeto S, Ferenci T. Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics. 2002;162:1055-62.
54. Barrick J, Yu D, Yoon S, Jeong H, Oh T, Schneider D, Lenski R, Kim J. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature. 2009;461:1243-7.
55. Jiang B, Argyros R, Bukowski J, Nelson S, Sharkey N, Kim S, Copeland V, Davidson RC, Chen R, Zhuang J, et al. Inactivation of a GAL4-like transcription factor improves cell fitness and product yield in glycoengineered Pichia pastoris strains. Appl Environ Microbiol. 2015;81:260-71.
56. Traven A, Jelicic B, Sopta M. Yeast Gal4: a transcriptional paradigm revisited. EMBO Rep. 2006;7:496-9.
57. MacPherson S, Larochelle M, Turcotte B. A fungal family of transcriptional regulators: the zinc cluster proteins. Microbiol Mol Biol Rev. 2006;70:583-604.
58. Alper H, Moxley J, Nevoigt E, Fink G, Stephanopoulos G. Engineering yeast transcription machinery for improved ethanol tolerance and production. Science. 2006;314:1565-8.
59. Hayashi M, Maeda T. Activation of the HOG pathway upon cold stress in Saccharomyces cerevisiae. J Biochem. 2006;139:797-803.
60. Bilsland E, Molin C, Swaminathan S, Ramne A, Sunnerhagen P. Rck1 and Rck2 MAPKAP kinases and the HOG pathway are required for oxidative stress resistance. Mol Microbiol. 2004;53:1743-56.
61. Schroer K, Peter Luef K, Stefan Hartner F, Glieder A, Pscheidt B. Engineering the Pichia pastoris methanol oxidation pathway for improved NADH regeneration during whole-cell biotransformation. Metab Eng. 2010;12:8-17.
62. Parks LW, Casey WM. Physiological implications of sterol biosynthesis in yeast. Annu Rev Microbiol. 1995;49:95-116.
63. Abe F, Hiraki T. Mechanistic role of ergosterol in membrane rigidity and cycloheximide resistance in Saccharomyces cerevisiae. Biochim Biophys Acta. 2009;1788:743-52.
64. Baumann K, Dato L, Graf AB, Frascotti G, Dragosits M, Porro D, Mattanovich D, Ferrer P, Branduardi P. The impact of oxygen on the transcriptome of recombinant S. cerevisiae and P. pastoris-a comparative analysis. BMC Genom. 2011;12:218.
65. Baumann K, Maurer M, Dragosits M, Cos O, Ferrer P, Mattanovich D. Hypoxic fed-batch cultivation of Pichia pastoris increases specific and volumetric productivity of recombinant proteins. Biotechnol Bioeng. 2008;100:177-83.
66. Baumann K, Adelantado N, Lang C, Mattanovich D, Ferrer P. Protein trafficking, ergosterol biosynthesis and membrane physics impact recombinant protein secretion in Pichia pastoris. Microb Cell Fact. 2011;10:93.
67. Jordà J, Jouhten P, Cámara E, Maaheimo H, Albiol J, Ferrer P. Metabolic flux profiling of recombinant protein secreting Pichia pastoris growing on glucose:methanol mixtures. Microb Cell Fact. 2012;11:57.