Evolutionary engineering improves tolerance for replacement jet fuels in Saccharomyces cerevisiae

Applied and Environmental Microbiology

Volumn 81, Issue 10, 2015, Pages 3316-3325

  Brennan, Timothy C R ^a   Williams, Thomas C ^a   Schulz, Benjamin L ^a   Palfreyman, Robin W ^a   Krömer, Jens O ^a   Nielsen, Lars K ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FUELS; HYDROCARBONS; JET FUEL; PROTEINS; STRAIN; YEAST;

EVOLUTIONARY ENGINEERING; FLAVOR AND FRAGRANCES; FUEL BLENDS; LIQUID HYDROCARBONS; MICROBIAL SYNTHESIS; PARENT STRAIN; SACCHAROMYCES CEREVISIAE STRAINS; TIME COURSE;

MONOTERPENES;

BIOENGINEERING; BIOFUEL; EVOLUTIONARY BIOLOGY; MONOTERPENE; MUTATION; PHENOTYPE; PROTEIN; TOLERANCE; YEAST;

SACCHAROMYCES CEREVISIAE;

CALCIUM BINDING PROTEIN; CYCLOHEXENE DERIVATIVE; HYDROCARBON; JP5 JET FUEL; LIMONENE; MEMBRANE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; TCB2 PROTEIN, S CEREVISIAE; TCB3 PROTEIN, S CEREVISIAE; TERPENE;

EVOLUTION; GENETICS; METABOLIC ENGINEERING; METABOLISM; SACCHAROMYCES CEREVISIAE;

BIOLOGICAL EVOLUTION; CALCIUM-BINDING PROTEINS; CYCLOHEXENES; HYDROCARBONS; MEMBRANE PROTEINS; METABOLIC ENGINEERING; MONOTERPENES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TERPENES;

EID: 84930018897     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.04144-14     Document Type: Article

References (42)

1. Keasling J. 2008. Synthetic biology for synthetic chemistry ACS Chem Biol 3:64-76. http://dx.doi.org/10.1021/cb7002434.
2. Brennan TCR, Turner CD, Krömer JO, Nielsen LK. 2012. Alleviating monoterpene toxicity using a two-phase extractive fermentation for the bioproduction of jet fuel mixtures in Saccharomyces cerevisiae Biotechnol Bioeng 109:2513-2522. http://dx.doi.org/10.1002/bit.24536.
3. Fischer MJC, Meyer S, Claudel P, Bergdoll M, Karst F. 2011. Metabolic engineering of monoterpene synthesis in yeast Biotechnol Bioeng 108:1883-1892. http://dx.doi.org/10.1002/bit.23129.
4. Lücker J, El Tamer MK, Schwab W, Verstappen FWA, van der Plas LHW, Bouwmeester HJ, Verhoeven HA. 2002. Monoterpene biosynthesis in lemon (Citrus limon) cDNA isolation and functional analysis of four monoterpene synthases. Eur J Biochem 269:3160-3171. http://dx.doi.org /10.1046/j.1432-1033.2002.02985.x.
5. Rico J, Pardo E, Orejas M. 2010. Enhanced production of a plant monoterpene by overexpression of the 3-hydroxy-3-methylglutaryl coenzyme A reductase catalytic domain in Saccharomyces cerevisiae Appl Environ Microbiol 76:6449-6454. http://dx.doi.org/10.1128/AEM.02987-09.
6. Chang M, Keasling J. 2006. Production of isoprenoid pharmaceuticals by engineered microbes Nat Chem Biol 2:674-681. http://dx.doi.org/10.1038/nchembio836.
7. Hill J, Nelson E, Tilman D, Polasky S, Tiffany D. 2006. Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels Proc Natl Acad Sci U S A 103:11206-11210. http://dx.doi.org/10.1073/pnas.0604600103.
8. Khor GK, Uzir MH. 2011. Saccharomyces cerevisiae: a potential stereospecific reduction tool for biotransformation of mono- and sesquiterpenoids Yeast 28:93-107. http://dx.doi.org/10.1002/yea.1827.
9. Sikkema J, de Bont JA, Poolman B. 1994. Interactions of cyclic hydrocarbons with biological membranes J Biol Chem 269:8022-8028.
10. Brennan TCR, Krömer JO, Nielsen LK. 2013. Physiological and transcriptional responses of Saccharomyces cerevisiae to d-limonene show changes to the cell wall but not to the plasma membrane Appl Environ Microbiol 79:3590-3600. http://dx.doi.org/10.1128/AEM.00463-13.
11. Hu F, Liu J, Du G, Hua Z, Zhou J, Chen J. 2012. Key cytomembrane ABC transporters of Saccharomyces cerevisiae fail to improve the tolerance to d-limonene Biotechnol Lett 34:1505-1509. http://dx.doi.org/10.1007/s10529-012-0931-6.
12. Çakar ZP, Turanli{dotless}-Yi{dotless}ldi{dotless}z B, Alki{dotless}m C, Yi{dotless}lmaz Ü . 2012. Evolutionary engineering of Saccharomyces cerevisiae for improved industrially important properties FEMS Yeast Res 12:171-182. http://dx.doi.org/10.1111/j .1567-1364.2011.00775.x.
13. Portnoy VA, Bezdan D, Zengler K. 2011. Adaptive laboratory evolution- harnessing the power of biology for metabolic engineering Curr Opin Biotechnol 22:590-594. http://dx.doi.org/10.1016/j.copbio.2011.03.007.
14. Atsumi S, Hanai T, Liao JC. 2008. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels Nature 451:86-89. http://dx.doi.org/10.1038/nature06450.
15. Brown SD, Guss AM, Karpinets TV, Parks JM, Smolin N, Yang S, Land ML, Klingeman DM, Bhandiwad A, Rodriguez M, Raman B, Shao X, Mielenz JR, Smith JC, Keller M, Lynd LR. 2011. Mutant alcohol dehydrogenase leads to improved ethanol tolerance in Clostridium thermocellum Proc Natl Acad Sci U S A 108:13752-13757. http://dx.doi.org/10.1073/pnas.1102444108.
16. Jantama K, Haupt MJ, Svoronos SA, Zhang X, Moore JC, Shanmugam KT, Ingram LO. 2008. Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate Biotechnol Bioeng 99:1140-1153. http://dx.doi.org/10.1002/bit.21694.
17. Wright J, Bellissimi E, de Hulster E, Wagner A, Pronk JT, van Maris AJA. 2011. Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae FEMS Yeast Res 11:299 -306. http://dx.doi.org/10.1111/j.1567-1364.2011.00719.x.
18. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Veronneau S, Dow S, Lucau-Danila A, Anderson K, Andre B, Arkin AP, Astromoff A, El-Bakkoury M, Bangham R, Benito R, Brachat S, Campanaro S, Curtiss M, Davis K, Deutschbauer A, Entian KD, Flaherty P, Foury F, Garfinkel DJ, Gerstein M, Gotte D, Guldener U, Hegemann JH, Hempel S, Herman Z, Jaramillo DF, Kelly DE, Kelly SL, Kotter P, LaBonte D, Lamb DC, Lan N, Liang H, Liao H, Liu L, Luo C, Lussier M, Mao R, Menard P, Ooi SL, Revuelta JL, Roberts CJ, Rose M, Ross-Macdonald P, Scherens B, et al. 2002. Functional profiling of the Saccharomyces cerevisiae genome Nature 418:387-391. http://dx.doi.org /10.1038/nature00935.
19. Atsumi S, Wu T-Y, Machado IMP, Huang W-C, Chen P-Y, Pellegrini M, Liao JC. 2010. Evolution, genomic analysis, and reconstruction of isobutanol tolerance in Escherichia coli Mol Syst Biol 6:449. http://dx.doi .org/10.1038/msb.2010.98.
20. Otero J, Vongsangnak W, Asadollahi M, Olivares-Hernandes R, Maury J, Farinelli L, Barlocher L, Osteras M, Schalk M, Clark A, Nielsen J. 2010. Whole genome sequencing of Saccharomyces cerevisiae: from genotype to phenotype for improved metabolic engineering applications.BMC Genomics 11:723. http://dx.doi.org/10.1186/1471-2164-11-723.
21. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2 Nat Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
22. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer Nat Biotechnol 29:24-26. http://dx.doi.org/10.1038/nbt.1754.
23. Cingolani P, Platts A, Wang LL, Coon M, Tung N, Wang L, Land SJ, Lu X, Ruden DM. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3 Fly 6:80-92. http://dx.doi .org/10.4161/fly.19695.
24. Solis-Escalante D, Kuijpers NGA, Bongaerts N, Bolat I, Bosman L, Pronk JT, Daran J-M, Daran-Lapujade P. 2013. amdSYM, a new dominant recyclable marker cassette for Saccharomyces cerevisiae FEMS Yeast Res 13:126-139. http://dx.doi.org/10.1111/1567-1364.12024.
25. Väremo L, Nielsen J, Nookaew I. 2013. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods Nucleic Acids Res 41:4378-4391. http://dx.doi.org/10.1093/nar/gkt111.
26. Schulz BL, Aebi M. 2009. Analysis of glycosylation site occupancy reveals a role for Ost3p and Ost6p in site-specific N-glycosylation efficiency Mol Cell Proteomics 8:357-364. http://dx.doi.org/10.1074/mcp.M800219-MCP200.
27. Bailey UM, Jamaluddin MF, Schulz BL. 2012. Analysis of congenital disorder of glycosylation-Id in a yeast model system shows diverse sitespecific under-glycosylation of glycoproteins J Proteome Res 11:5376-5383. http://dx.doi.org/10.1021/pr300599f.
28. Gillet LC, Navarro P, Tate S, Rost H, Selevsek N, Reiter L, Bonner R, Aebersold R. 2012. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis Mol Cell Proteomics 11:O111.016717. http://dx.doi.org/10.1074/mcp.O111.016717.
29. Liu Y, Chen J, Sethi A, Li QK, Chen L, Collins B, Gillet LC, Wollscheid B, Zhang H, Aebersold R. 2014. Glycoproteomic analysis of prostate cancer tissues by SWATH mass spectrometry discovers N-acylethanolamine acid amidase and protein tyrosine kinase 7 as signatures for tumor aggressiveness Mol Cell Proteomics 13:1753-1768. http://dx.doi.org/10.1074/mcp.M114.038273.
30. Sullivan M, Li S, Aroney S, Deng B, Li C, Roura E, Schulz B, Harcourt B, Forbes J, Gilbert R. 2015. A rapid extraction method for glycogen from formalin-fixed liver Carbohydr Polym 118:9-15. http://dx.doi.org/10.1016/j.carbpol.2014.11.005.
31. Choi M, Chang C-Y, Vitek O. 20 September 2013. Package 'MSstats.' Protein significance analysis in LC-MS, SRM and DIA for label-free or label-based proteomics experiments, version 2.0.1. http://www .bioconductor.org/packages/2.13/bioc/manuals/MSstats/man/MSstats .pdf.
32. Manford AG, Stefan CJ, Yuan HL, MacGurn JA, Emr SD. 2012. ER-toplasma membrane tethering proteins regulate cell signaling and ER morphology Dev Cell 23:1129-1140. http://dx.doi.org/10.1016/j.devcel.2012.11.004.
33. Creutz CE, Snyder SL, Schulz TA. 2004. Characterization of the yeast tricalbins: membrane-bound multi-C2-domain proteins that form complexes involved in membrane trafficking Cell Mol Life Sci 61:1208-1220. http://dx.doi.org/10.1007/s00018-004-4029-8.
34. Ram AF, Klis FM. 2006. Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red Nat Protoc 1:2253-2256. http://dx.doi.org/10.1038/nprot.2006.397.
35. Levin DE. 2011. Regulation of cell wall biogenesis in Saccharomyces cerevisiae:the cell wall integrity signaling pathway Genetics 189:1145-1175. http://dx.doi.org/10.1534/genetics.111.128264.
36. Dowell RD, Ryan O, Jansen A, Cheung D, Agarwala S, Danford T, Bernstein DA, Rolfe PA, Heisler LE, Chin B, Nislow C, Giaever G, Phillips PC, Fink GR, Gifford DK, Boone C. 2010. Genotype to phenotype: a complex problem Science 328:469. http://dx.doi.org/10.1126/science.1189015.
37. Moukadiri I, Armero J, Abad A, Sentandreu R, Zueco J. 1997. Identification of a mannoprotein present in the inner layer of the cell wall of Saccharomyces cerevisiae J Bacteriol 179:2154-2162.
38. Mrsa V, Ecker M, Strahl-Bolsinger S, Nimtz M, Lehle L, Tanner W. 1999. Deletion of new covalently linked cell wall glycoproteins alters the electrophoretic mobility of phosphorylated wall components of Saccharomyces cerevisiae J Bacteriol 181:3076-3086.
39. Toulmay A, Prinz WA. 2012. A conserved membrane-binding domain targets proteins to organelle contact sites J Cell Sci 125:49-58. http://dx .doi.org/10.1242/jcs.085118.
40. Bishop JR, Nelson G, Lamb J. 1998. Microencapsulation in yeast cells J Microencapsul 15:761-773. http://dx.doi.org/10.3109/02652049809008259.
41. Ciamponi F, Duckham C, Tirelli N. 2012. Yeast cells as microcapsules Analytical tools and process variables in the encapsulation of hydrophobes in S. cerevisiae. Appl Microbiol Biotechnol 95:1445-1456. http://dx.doi .org/10.1007/s00253-012-4127-8.
42. Amyris. 19 June 2012. Photo release-Azul Brazilian Airlines makes successful demonstration flight with Amyris renewable jet fuel produced from sugarcane. [Press release.] Retrieved from https://amyris.com/photo -release-azul-brazilian-airlines-makes-successful-demonstration-flight -with-amyris-renewable-jet-fuel-produced-from-sugarcane/.