Engineering the thermotolerant industrial yeast Kluyveromyces marxianus for anaerobic growth

Metabolic Engineering - Tập 67 - Trang 347-364 - 2021
Wijbrand J.C. Dekker1, Raúl A. Ortiz-Merino1, Astrid Kaljouw1, Julius Battjes1, Frank W. Wiering1, Christiaan Mooiman1, Pilar de la Torre1, Jack T. Pronk1
1Department of Biotechnology, Delft University of Technology, Van der Maasweg 9, 2629 HZ, Delft, the Netherlands

Tài liệu tham khảo

Alimardani, 2004, SUT1-promoted sterol uptake involves the ABC transporter Aus1 and the mannoprotein Dan1 whose synergistic action is sufficient for this process, Biochem. J., 381, 195, 10.1042/BJ20040297 Andreasen, 1953, Anaerobic nutrition of Saccharomyces cerevisiae I. Ergosterol requirement for growth in a defined medium, J. Cell. Physiol., 41, 23, 10.1002/jcp.1030410103 Andreasen, 1953, Anaerobic nutrition of Saccharomyces cerevisiae II. Unsaturated fatty acid requirement for growth in a defined medium, J. Cell. Physiol., 43, 271, 10.1002/jcp.1030430303 Annual World Fuel Ethanol Production, 2020, Renew. Fuels Assoc. Auwera, 2013, From FastQ data to high‐confidence variant calls: the genome analysis Toolkit best practices pipeline, Curr. Protoc. Bioinforma., 43, 11, 10.1002/0471250953.bi1110s43 Bakker, 2001, Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae, FEMS Microbiol. Rev., 25, 15, 10.1111/j.1574-6976.2001.tb00570.x Bankevich, 2012, SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J. Comput. Biol., 19, 455, 10.1089/cmb.2012.0021 Black, 2007, Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation, Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 1771, 286, 10.1016/j.bbalip.2006.05.003 Blomqvist, 2012, Physiological requirements for growth and competitveness of Dekkera bruxellensis under oxygen limited or anaerobic conditions, Yeast, 29, 265, 10.1002/yea.2904 Boender, 2009, Quantitative physiology of Saccharomyces cerevisiae at near-zero specific growth rates, Appl. Environ. Microbiol., 75, 5607, 10.1128/AEM.00429-09 Bracher, 2017, Laboratory evolution of a biotin-requiring Saccharomyces cerevisiae strain for full biotin prototrophy and identification of causal mutations, Appl. Environ. Microbiol., 83, 1, 10.1128/AEM.00892-17 Choudhary, 2016, Thermotolerant fermenting yeasts for simultaneous saccharification fermentation of lignocellulosic biomass, Electron. J. Biotechnol., 21, 82, 10.1016/j.ejbt.2016.02.007 Cingolani, 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, 10.4161/fly.19695 da Costa, 2018, Anaerobiosis revisited: growth of Saccharomyces cerevisiae under extremely low oxygen availability, Appl. Microbiol. Biotechnol., 102, 2101, 10.1007/s00253-017-8732-4 Daran-Lapujade, 2008, Chemostat-based micro-array analysis in baker's yeast, 257, 10.1016/S0065-2911(08)00004-0 Dashko, 2014, Why, when, and how did yeast evolve alcoholic fermentation?, FEMS Yeast Res., 14, 826, 10.1111/1567-1364.12161 Dekker, 2019, Anaerobic growth of Saccharomyces cerevisiae CEN.PK113-7D does not depend on synthesis or supplementation of unsaturated fatty acids, FEMS Yeast Res., 19, 10.1093/femsyr/foz060 Entian, 2007, 25 yeast genetic strain and plasmid collections, 629, 10.1016/S0580-9517(06)36025-4 Favaro, 2019, Exploring industrial and natural Saccharomyces cerevisiae strains for the bio-based economy from biomass: the case of bioethanol, Crit. Rev. Biotechnol., 39, 800, 10.1080/07388551.2019.1619157 Fonseca, 2008, The yeast Kluyveromyces marxianus and its biotechnological potential, Appl. Microbiol. Biotechnol., 79, 339, 10.1007/s00253-008-1458-6 Gietz, 2001, Genetic transformation of yeast, Biotechniques, 30, 816, 10.2144/01304rv02 Gojković, 2004, Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts, Mol. Genet. Genom., 271, 387, 10.1007/s00438-004-0995-7 Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Gu, 2016, Complex heatmaps reveal patterns and correlations in multidimensional genomic data, Bioinformatics, 32, 2847, 10.1093/bioinformatics/btw313 Guo, 2020, Engineering microbial cell morphology and membrane homeostasis toward industrial applications, Curr. Opin. Biotechnol., 66, 18, 10.1016/j.copbio.2020.05.004 Hassing, 2019, Connecting central carbon and aromatic amino acid metabolisms to improve de novo 2-phenylethanol production in Saccharomyces cerevisiae, Metab. Eng., 56, 165, 10.1016/j.ymben.2019.09.011 Hong, 2007, Construction of thermotolerant yeast expressing thermostable cellulase genes, J. Biotechnol., 130, 114, 10.1016/j.jbiotec.2007.03.008 Hughes, 2013, Automated UV-C mutagenesis of Kluyveromyces marxianus NRRL Y-1109 and selection for microaerophilic growth and ethanol production at elevated temperature on biomass sugars, J. Lab. Autom., 18, 276, 10.1177/2211068213480037 Jacquier, 2010, Ypk1, the yeast orthologue of the human serum- and glucocorticoid-induced kinase, is required for efficient uptake of fatty acids, J. Cell Sci., 123, 2218, 10.1242/jcs.063073 Jansen, 2017, Saccharomyces cerevisiae strains for second-generation ethanol production: from academic exploration to industrial implementation, FEMS Yeast Res., 17, 1, 10.1093/femsyr/fox044 Jeong, 2012, Genome sequence of the thermotolerant yeast Kluyveromyces marxianus var. marxianus KCTC 17555, Eukaryot. Cell, 11, 1584, 10.1128/EC.00260-12 Jones, 2014, InterProScan 5: genome-scale protein function classification, Bioinformatics, 30, 1236, 10.1093/bioinformatics/btu031 Jordá, 2020, Regulation of ergosterol biosynthesis in Saccharomyces cerevisiae, Genes, 11, 795, 10.3390/genes11070795 Juergens, 2018, Evaluation of a novel cloud-based software platform for structured experiment design and linked data analytics, Sci. Data, 5, 1, 10.1038/sdata.2018.195 Kiers, 1998, Regulation of alcoholic fermentation in batch and chemostat cultures of Kluyveromyces lactis CBS 2359, Yeast, 14, 459, 10.1002/(SICI)1097-0061(19980330)14:5<459::AID-YEA248>3.0.CO;2-O Kolmogorov, 2019, Assembly of long, error-prone reads using repeat graphs, Nat. Biotechnol., 37, 540, 10.1038/s41587-019-0072-8 Koren, 2017, Canu: scalable and accurate long-read assembly via adaptive κ-mer weighting and repeat separation, Genome Res., 27, 722, 10.1101/gr.215087.116 Laman Trip, 2020, Yeasts collectively extend the limits of habitable temperatures by secreting glutathione, Nat. Microbiol., 5, 943, 10.1038/s41564-020-0704-2 Landry, 2012, F-box protein specificity for G1 cyclins is dictated by subcellular localization, PLoS Genet., 8, 10.1371/journal.pgen.1002851 Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol., 10, 10.1186/gb-2009-10-3-r25 Lechner, 2011, Proteinortho: detection of (Co-)orthologs in large-scale analysis, BMC Bioinf., 12, 124, 10.1186/1471-2105-12-124 Lee, 2015, A highly characterized yeast Toolkit for modular, multipart assembly, ACS Synth. Biol., 4, 975, 10.1021/sb500366v Li, 2009, Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, 25, 1754, 10.1093/bioinformatics/btp324 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Liao, 2014, FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Lorenz, 2011, ViennaRNA package 2.0, Algorithm Mol. Biol., 6, 26, 10.1186/1748-7188-6-26 Madeira, 2018, Towards high-temperature fuel ethanol production using Kluyveromyces marxianus: on the search for plug-in strains for the Brazilian sugarcane-based biorefinery, Biomass Bioenergy, 119, 217, 10.1016/j.biombioe.2018.09.010 Mans, 2015, CRISPR/Cas9: a molecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae, FEMS Yeast Res., 15, 1, 10.1093/femsyr/fov004 Marek, 2011, The yeast plasma membrane ATP binding cassette (ABC) transporter Aus1: purification, characterization, and the effect of lipids on its activity, J. Biol. Chem., 286, 21835, 10.1074/jbc.M111.244525 Marek, 2014, Serum albumin promotes ATP-binding cassette transporter-dependent sterol uptake in yeast, FEMS Yeast Res., 14, 1223, 10.1111/1567-1364.12219 Mashego, 2003, Critical evaluation of sampling techniques for residual glucose determination in carbon-limited chemostat culture of Saccharomyces cerevisiae, Biotechnol. Bioeng., 83, 395, 10.1002/bit.10683 McCarthy, 2012, Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation, Nucleic Acids Res., 40, 4288, 10.1093/nar/gks042 Mejía-Barajas, 2018, Second-Generation bioethanol production through a simultaneous saccharification-fermentation process using Kluyveromyces marxianus thermotolerant yeast Merico, 2007, Fermentative lifestyle in yeasts belonging to the Saccharomyces complex, FEBS J., 274, 976, 10.1111/j.1742-4658.2007.05645.x Mooiman, 2021, Critical parameters and procedures for anaerobic cultivation of yeasts in bioreactors and anaerobic chambers, FEMS Yeast Res., 21, 1, 10.1093/femsyr/foab035 Nagy, 1992, Divergent evolution of pyrimidine biosynthesis between anaerobic and aerobic yeasts, Proc. Natl. Acad. Sci. U. S. A, 89, 8966, 10.1073/pnas.89.19.8966 Nijkamp, 2012, De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology, Microb. Cell Factories, 11, 36, 10.1186/1475-2859-11-36 Ortiz-Merino, 2018, Ploidy variation in Kluyveromyces marxianus separates dairy and non-dairy isolates, Front. Genet., 9, 1, 10.3389/fgene.2018.00094 Palmer, 2019 Papapetridis, 2018, Optimizing anaerobic growth rate and fermentation kinetics in Saccharomyces cerevisiae strains expressing Calvin-cycle enzymes for improved ethanol yield, Biotechnol. Biofuels, 11, 1, 10.1186/s13068-017-1001-z Passi, 1993, Saturated dicarboxylic acids as products of unsaturated fatty acid oxidation, Biochim. Biophys. Acta Lipids Lipid. Metabol., 1168, 190, 10.1016/0005-2760(93)90124-R Perli, 2020, Vitamin requirements and biosynthesis in Saccharomyces cerevisiae, Yeast, 1 Postma, 1989, Enzymic analysis of the crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae, Appl. Environ. Microbiol., 55, 468, 10.1128/aem.55.2.468-477.1989 R Core Team, 2017 Rajkumar, 2019, Biological parts for Kluyveromyces marxianus synthetic biology, Front. Bioeng. Biotechnol., 7, 1, 10.3389/fbioe.2019.00097 Riley, 2016, Comparative genomics of biotechnologically important yeasts, Proc. Natl. Acad. Sci. U. S. A, 113, 9882, 10.1073/pnas.1603941113 Robinson, 2010, A scaling normalization method for differential expression analysis of RNA-seq data, Genome Biol., 11, 10.1186/gb-2010-11-3-r25 Rouwenhorst, 1988, Production, distribution, and kinetic properties of inulinase in continuous cultures of Kluyveromyces marxianus CBS 6556, Appl. Environ. Microbiol., 54, 1131, 10.1128/aem.54.5.1131-1137.1988 Schüller, 2003, Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae, Curr. Genet., 43, 139, 10.1007/s00294-003-0381-8 Seret, 2009, Combined phylogeny and neighborhood analysis of the evolution of the ABC transporters conferring multiple drug resistance in hemiascomycete yeasts, BMC Genom., 10, 459, 10.1186/1471-2164-10-459 Shi, 1998, Anaerobic growth and improved fermentation of Pichia stipitis bearing a URA1 gene from Saccharomyces cerevisiae, Appl. Microbiol. Biotechnol., 50, 339, 10.1007/s002530051301 Snoek, 2007, Factors involved in anaerobic growth of Saccharomyces cerevisiae, Yeast, 24, 1, 10.1002/yea.1430 Snoek, 2006, Why does Kluyveromyces lactis not grow under anaerobic conditions? Comparison of essential anaerobic genes of Saccharomyces cerevisiae with the Kluyveromyces lactis genome, FEMS Yeast Res., 6, 393, 10.1111/j.1567-1364.2005.00007.x Solis-Escalante, 2013, amdSYM, A new dominant recyclable marker cassette for Saccharomyces cerevisiae, FEMS Yeast Res., 13, 126, 10.1111/1567-1364.12024 Stovicek, 2017, CRISPR/Cas system for yeast genome engineering: advances and applications, FEMS Yeast Res., 17, 1, 10.1093/femsyr/fox030 Tai, 2005, Two-dimensional transcriptome analysis in chemostat cultures: combinatorial effects of oxygen availability and macronutrient limitation in Saccharomyces cerevisiae, J. Biol. Chem., 280, 437, 10.1074/jbc.M410573200 Takishita, 2012, Lateral transfer of tetrahymanol-synthesizing genes has allowed multiple diverse eukaryote lineages to independently adapt to environments without oxygen, Biol. Direct, 7, 5, 10.1186/1745-6150-7-5 Tetsuya, 2013, Bioethanol production from lignocellulosic biomass by a novel Kluyveromyces marxianus strain, Biosci. Biotechnol. Biochem., 77, 1505, 10.1271/bbb.130173 Thorwall, 2020, Stress-tolerant non-conventional microbes enable next-generation chemical biosynthesis, Nat. Chem. Biol., 16, 113, 10.1038/s41589-019-0452-x Van Eunen, 2010, Measuring enzyme activities under standardized in vivo-like conditions for systems biology, FEBS J., 277, 749, 10.1111/j.1742-4658.2009.07524.x van Urk, 1989, Glucose transport in crabtree-positive and crabtree-negative yeasts, J. Gen. Microbiol., 135, 2399 Väremo, 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, 10.1093/nar/gkt111 Verduyn, 1990, Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures, J. Gen. Microbiol., 136, 395, 10.1099/00221287-136-3-395 Visser, 1990, Oxygen requirements of yeasts, Appl. Environ. Microbiol., 56, 3785, 10.1128/aem.56.12.3785-3792.1990 von Meyenburg, 1969, Katabolit-Repression und der Sprossungszyklus von Saccharomyces cerevisiae, ETH Zürich Walker, 2014, Pilon : an integrated tool for comprehensive microbial variant detection and genome assembly improvement, PloS One, 9, 10.1371/journal.pone.0112963 Weusthuis, 2011, Microbial production of bulk chemicals: development of anaerobic processes, Trends Biotechnol., 29, 153, 10.1016/j.tibtech.2010.12.007 Weusthuis, 1994, Effects of oxygen limitation on sugar metabolism in yeasts: a continuous-culture study of the Kluyver effect, Microbiology, 140, 703, 10.1099/00221287-140-4-703 Wiersma, 2020, Squalene-tetrahymanol cyclase expression enables sterol-independent growth of Saccharomyces cerevisiae, Appl. Environ. Microbiol., 86, 1, 10.1128/AEM.00672-20 Wilcox, 2002, Transcriptional profiling identifies two members of the ATP-binding cassette transporter superfamily required for sterol uptake in yeast, J. Biol. Chem., 277, 32466, 10.1074/jbc.M204707200 Wilkins, 2008, Fermentation of xylose by the thermotolerant yeast strains Kluyveromyces marxianus IMB2, IMB4, and IMB5 under anaerobic conditions, Process Biochem., 43, 346, 10.1016/j.procbio.2007.12.011 Zavrel, 2013, Comparison of sterol import under aerobic and anaerobic conditions in three fungal species, Candida albicans, Candida glabrata, and Saccharomyces cerevisiae, Eukaryot. Cell, 12, 725, 10.1128/EC.00345-12