Optimized genome-wide CRISPR screening enables rapid engineering of growth-based phenotypes in Yarrowia lipolytica

Robertson, Nicholas R.; Trivedi, Varun; Lupish, Brian; Ramesh, Adithya; Aguilar, Yuna; Carrera, Stephanie; Lee, Sangcheon; Arteaga, Anthony; Nguyen, Alexander; Lenert-Mondou, Chase; Harland-Dunaway, Marcus; Jinkerson, Robert; Wheeldon, Ian

doi:10.1016/j.ymben.2024.09.005

Title: Optimized genome-wide CRISPR screening enables rapid engineering of growth-based phenotypes in Yarrowia lipolytica

Journal Article · 01 November 2024 · Metabolic Engineering

DOI: https://doi.org/10.1016/j.ymben.2024.09.005 · OSTI ID:2446998

Robertson, Nicholas R.; Trivedi, Varun; Lupish, Brian; Ramesh, Adithya; Aguilar, Yuna; Carrera, Stephanie; Lee, Sangcheon; Arteaga, Anthony; Nguyen, Alexander; Lenert-Mondou, Chase; Harland-Dunaway, Marcus; Jinkerson, Robert;

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Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0019093

OSTI ID:: 2446998

Journal Information:: Metabolic Engineering, Journal Name: Metabolic Engineering Journal Issue: C Vol. 86; ISSN 1096-7176

Publisher:: ElsevierCopyright Statement

Country of Publication:: Belgium

Language:: English

References (70)

Multiplexed CRISPR Activation of Cryptic Sugar Metabolism Enables Yarrowia Lipolytica Growth on Cellobiose Schwartz, Cory; Curtis, Nicholas; Löbs, Ann-Kathrin Biotechnology Journal, Vol. 13, Issue 9 https://doi.org/10.1002/biot.201700584	journal	May 2018
CRISPRi repression of nonhomologous end-joining for enhanced genome engineering via homologous recombination in Yarrowia lipolytica Schwartz, Cory; Frogue, Keith; Ramesh, Adithya Biotechnology and Bioengineering, Vol. 114, Issue 12 https://doi.org/10.1002/bit.26404	journal	September 2017
Genome‐wide CRISPR‐Cas9 screen reveals a persistent null‐hyphal phenotype that maintains high carotenoid production in Yarrowia lipolytica Lupish, Brian; Hall, Jordan; Schwartz, Cory Biotechnology and Bioengineering, Vol. 119, Issue 12 https://doi.org/10.1002/bit.28219	journal	September 2022
Guide RNA Design for Genome-Wide CRISPR Screens in Yarrowia lipolytica Ramesh, Adithya; Wheeldon, Ian Yarrowia lipolytica https://doi.org/10.1007/978-1-0716-1414-3_8	book	April 2021
Protein-O-mannosyltransferases in virulence and development Lengeler, K. B.; Tielker, D.; Ernst, J. F. Cellular and Molecular Life Sciences, Vol. 65, Issue 4 https://doi.org/10.1007/s00018-007-7409-z	journal	November 2007
Dimorphism and hydrocarbon metabolism in Yarrowia lipolytica var. indica Palande, A. S.; Kulkarni, S. V.; León-Ramirez, C. Archives of Microbiology, Vol. 196, Issue 8 https://doi.org/10.1007/s00203-014-0990-2	journal	May 2014
The acuH gene of Aspergillus nidulans , required for growth on acetate and long-chain fatty acids, encodes a putative homologue of the mammalian carnitine/acylcarnitine carrier De Lucas, J. Ramón; Domínguez, A. I.; Valenciano, Susana Archives of Microbiology, Vol. 171, Issue 6 https://doi.org/10.1007/s002030050725	journal	May 1999
Genetic engineering of an industrial yeast Candida glycerinogenes for efficient production of 2-phenylethanol Wang, Yuqin; Zhang, Zhongyuan; Lu, Xinyao Applied Microbiology and Biotechnology, Vol. 104, Issue 24 https://doi.org/10.1007/s00253-020-10991-4	journal	November 2020
One-step transformation of the dimorphic yeast Yarrowia lipolytica Chen, D.-C.; Beckerich, J.-M.; Gaillardin, C. Applied Microbiology and Biotechnology, Vol. 48, Issue 2, p. 232-235 https://doi.org/10.1007/s002530051043	journal	August 1997
Yeast genetic interaction screens in the age of CRISPR/Cas Adames, Neil R.; Gallegos, Jenna E.; Peccoud, Jean Current Genetics, Vol. 65, Issue 2 https://doi.org/10.1007/s00294-018-0887-8	journal	September 2018
Functional analysis and subcellular localization of two geranylgeranyl diphosphate synthases from Penicillium paxilli Saikia, Sanjay; Scott, Barry Molecular Genetics and Genomics, Vol. 282, Issue 3 https://doi.org/10.1007/s00438-009-0463-5	journal	June 2009
EasyClone 2.0: expanded toolkit of integrative vectors for stable gene expression in industrial Saccharomyces cerevisiae strains Stovicek, Vratislav; Borja, Gheorghe M.; Forster, Jochen Journal of Industrial Microbiology and Biotechnology, Vol. 42, Issue 11 https://doi.org/10.1007/s10295-015-1684-8	journal	November 2015
Utilization of n-alkane and roles of lipid transfer proteins in Yarrowia lipolytica Fukuda, Ryouichi World Journal of Microbiology and Biotechnology, Vol. 39, Issue 4 https://doi.org/10.1007/s11274-023-03541-3	journal	February 2023
Cloning and characterization of the Saccharomyces cerevisiae C-22 sterol desaturase gene, encoding a second cytochrome P-450 involved in ergosterol biosynthesis Skaggs, B. A.; Alexander, J. F.; Pierson, C. A. Gene, Vol. 169, Issue 1 https://doi.org/10.1016/0378-1119(95)00770-9	journal	February 1996
Protein disulfide isomerase is a component of the microsomal triglyceride transfer protein complex. Wetterau, J. R.; Combs, K. A.; Spinner, S. N. Journal of Biological Chemistry, Vol. 265, Issue 17 https://doi.org/10.1016/S0021-9258(19)38742-3	journal	June 1990
Isolation of bioactive peptides from tryptone that modulate lipase production in Yarrowia lipolytica Turki, Saoussen; Kraeim, Ines Ben; Weeckers, Frederic Bioresource Technology, Vol. 100, Issue 10 https://doi.org/10.1016/j.biortech.2008.12.053	journal	May 2009
Efficient Multiplexed Integration of Synergistic Alleles and Metabolic Pathways in Yeasts via CRISPR-Cas Horwitz, Andrew A.; Walter, Jessica M.; Schubert, Max G. Cell Systems, Vol. 1, Issue 1 https://doi.org/10.1016/j.cels.2015.02.001	journal	July 2015
Hydrophobic substrate utilisation by the yeast Yarrowia lipolytica, and its potential applications Fickers, P.; Benetti, P.; Wache, Y. FEMS Yeast Research, Vol. 5, Issue 6-7, p. 527-543 https://doi.org/10.1016/j.femsyr.2004.09.004	journal	April 2005
Metabolic activity in dormant conidia of Aspergillus niger and developmental changes during conidial outgrowth Novodvorska, Michaela; Stratford, Malcolm; Blythe, Martin J. Fungal Genetics and Biology, Vol. 94, p. 23-31 https://doi.org/10.1016/j.fgb.2016.07.002	journal	September 2016
A Complex of Pdi1p and the Mannosidase Htm1p Initiates Clearance of Unfolded Glycoproteins from the Endoplasmic Reticulum Gauss, Robert; Kanehara, Kazue; Carvalho, Pedro Molecular Cell, Vol. 42, Issue 6 https://doi.org/10.1016/j.molcel.2011.04.027	journal	June 2011
Solid state fermentation for the production of γ-decalactones by Yarrowia lipolytica Try, Sophal; De-Coninck, Joëlle; Voilley, Andrée Process Biochemistry, Vol. 64, p. 9-15 https://doi.org/10.1016/j.procbio.2017.10.004	journal	October 2017
Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae Jakočiūnas, Tadas; Bonde, Ida; Herrgård, Markus Metabolic Engineering, Vol. 28 https://doi.org/10.1016/j.ymben.2015.01.008	journal	March 2015
Genome scale engineering techniques for metabolic engineering Liu, Rongming; Bassalo, Marcelo C.; Zeitoun, Ramsey I. Metabolic Engineering, Vol. 32 https://doi.org/10.1016/j.ymben.2015.09.013	journal	November 2015
Functional genomics for the oleaginous yeast Yarrowia lipolytica Patterson, Kurt; Yu, James; Landberg, Jenny Metabolic Engineering, Vol. 48 https://doi.org/10.1016/j.ymben.2018.05.008	journal	July 2018
Validating genome-wide CRISPR-Cas9 function improves screening in the oleaginous yeast Yarrowia lipolytica Schwartz, Cory; Cheng, Jan-Fang; Evans, Robert Metabolic Engineering, Vol. 55 https://doi.org/10.1016/j.ymben.2019.06.007	journal	September 2019
Genome-wide host-pathway interactions affecting cis-cis-muconic acid production in yeast Cachera, Paul; Kurt, Nikolaj Can; Røpke, Andreas Metabolic Engineering, Vol. 83, p. 75-85 https://doi.org/10.1016/j.ymben.2024.02.015	journal	May 2024
Genome-Wide CRISPRi-Based Identification of Targets for Decoupling Growth from Production Li, Songyuan; Jendresen, Christian Bille; Landberg, Jenny ACS Synthetic Biology, Vol. 9, Issue 5 https://doi.org/10.1021/acssynbio.9b00143	journal	April 2020
Host-Informed Expression of CRISPR Guide RNA for Genomic Engineering in Komagataella phaffii Dalvie, Neil C.; Leal, Justin; Whittaker, Charles A. ACS Synthetic Biology, Vol. 9, Issue 1 https://doi.org/10.1021/acssynbio.9b00372	journal	December 2019
Mechanism of Assembling Isoprenoid Building Blocks 1. Elucidation of the Structural Motifs for Substrate Binding in Geranyl Pyrophosphate Synthase Liu, Zhihong; Zhou, Jingwei; Wu, Ruibo Journal of Chemical Theory and Computation, Vol. 10, Issue 11, p. 5057-5067 https://doi.org/10.1021/ct500607n	journal	October 2014
Multi-functional genome-wide CRISPR system for high throughput genotype–phenotype mapping Lian, Jiazhang; Schultz, Carl; Cao, Mingfeng Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13621-4	journal	December 2019
Combinatorial CRISPR screen identifies fitness effects of gene paralogues Thompson, Nicola A.; Ranzani, Marco; van der Weyden, Louise Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21478-9	journal	February 2021
CRISPR-assisted rational flux-tuning and arrayed CRISPRi screening of an l-proline exporter for l-proline hyperproduction Liu, Jiao; Liu, Moshi; Shi, Tuo Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28501-7	journal	February 2022
Genome-wide functional screens enable the prediction of high activity CRISPR-Cas9 and -Cas12a guides in Yarrowia lipolytica Baisya, Dipankar; Ramesh, Adithya; Schwartz, Cory Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-28540-0	journal	February 2022
Stress-tolerant non-conventional microbes enable next-generation chemical biosynthesis Thorwall, Sarah; Schwartz, Cory; Chartron, Justin W. Nature Chemical Biology, Vol. 16, Issue 2 https://doi.org/10.1038/s41589-019-0452-x	journal	January 2020
Bioinformatic mapping of a more precise Aspergillus niger degradome Dong, Zixing; Yang, Shuangshuang; Lee, Byong H. Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-020-80028-3	journal	January 2021
An inducible CRISPR interference library for genetic interrogation of Saccharomyces cerevisiae biology Momen-Roknabadi, Amir; Oikonomou, Panos; Zegans, Maxwell Communications Biology, Vol. 3, Issue 1 https://doi.org/10.1038/s42003-020-01452-9	journal	November 2020
acCRISPR: an activity-correction method for improving the accuracy of CRISPR screens Ramesh, Adithya; Trivedi, Varun; Lee, Sangcheon Communications Biology, Vol. 6, Issue 1 https://doi.org/10.1038/s42003-023-04996-8	journal	June 2023
Microfluidic screening and whole-genome sequencing identifies mutations associated with improved protein secretion by yeast Huang, Mingtao; Bai, Yunpeng; Sjostrom, Staffan L. Proceedings of the National Academy of Sciences, Vol. 112, Issue 34 https://doi.org/10.1073/pnas.1506460112	journal	August 2015
RNAi expression tuning, microfluidic screening, and genome recombineering for improved protein production in Saccharomyces cerevisiae Wang, Guokun; Björk, Sara M.; Huang, Mingtao Proceedings of the National Academy of Sciences, Vol. 116, Issue 19 https://doi.org/10.1073/pnas.1820561116	journal	April 2019
Bidirectional titration of yeast gene expression using a pooled CRISPR guide RNA approach Bowman, Emily K.; Deaner, Matthew; Cheng, Jan-Fang Proceedings of the National Academy of Sciences, Vol. 117, Issue 31 https://doi.org/10.1073/pnas.2007413117	journal	July 2020
The Saccharomyces cerevisiae Protein Mnn10p/Bed1p Is a Subunit of a Golgi Mannosyltransferase Complex Jungmann, Joern; Rayner, Julian C.; Munro, Sean Journal of Biological Chemistry, Vol. 274, Issue 10 https://doi.org/10.1074/jbc.274.10.6579	journal	March 1999
Ubp15p, a Ubiquitin Hydrolase Associated with the Peroxisomal Export Machinery Debelyy, Mykhaylo O.; Platta, Harald W.; Saffian, Delia Journal of Biological Chemistry, Vol. 286, Issue 32 https://doi.org/10.1074/jbc.M111.238600	journal	June 2011
Saccharomyces cerevisiae Acyl-CoA Oxidase Follows a Novel, Non-PTS1, Import Pathway into Peroxisomes That Is Dependent on Pex5p Klein, André T. J.; van den Berg, Marlene; Bottger, Gina Journal of Biological Chemistry, Vol. 277, Issue 28 https://doi.org/10.1074/jbc.M203254200	journal	April 2002
Identification and Characterization of aSaccharomyces cerevisiae Gene, RSB1, Involved in Sphingoid Long-chain Base Release Kihara, Akio; Igarashi, Yasuyuki Journal of Biological Chemistry, Vol. 277, Issue 33 https://doi.org/10.1074/jbc.M203385200	journal	August 2002
A Membrane Coat Complex Essential for Endosome-to-Golgi Retrograde Transport in Yeast Seaman, Matthew N. J.; Michael McCaffery, J.; Emr, Scott D. The Journal of Cell Biology, Vol. 142, Issue 3 https://doi.org/10.1083/jcb.142.3.665	journal	August 1998
Eb1 Proteins Regulate Microtubule Dynamics, Cell Polarity, and Chromosome Stability Tirnauer, Jennifer S.; Bierer, Barbara E. Journal of Cell Biology, Vol. 149, Issue 4 https://doi.org/10.1083/jcb.149.4.761	journal	May 2000
Parallel phospholipid transfer by Vps13 and Atg2 determines autophagosome biogenesis dynamics Dabrowski, Rahel; Tulli, Susanna; Graef, Martin Journal of Cell Biology, Vol. 222, Issue 7 https://doi.org/10.1083/jcb.202211039	journal	April 2023
Vps52p, Vps53p, and Vps54p Form a Novel Multisubunit Complex Required for Protein Sorting at the Yeast Late Golgi Conibear, Elizabeth; Stevens, Tom H. Molecular Biology of the Cell, Vol. 11, Issue 1 https://doi.org/10.1091/mbc.11.1.305	journal	January 2000
A data library of Candida albicans functional genomic screens Gervais, Nicholas C.; Halder, Viola; Shapiro, Rebecca S. FEMS Yeast Research, Vol. 21, Issue 7 https://doi.org/10.1093/femsyr/foab060	journal	November 2021
Analyzing CRISPR screens in non-conventional microbes Trivedi, Varun; Ramesh, Adithya; Wheeldon, Ian Journal of Industrial Microbiology and Biotechnology, Vol. 50, Issue 1 https://doi.org/10.1093/jimb/kuad006	journal	February 2023
The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update Afgan, Enis; Baker, Dannon; Batut, Bérénice Nucleic Acids Research, Vol. 46, Issue W1 https://doi.org/10.1093/nar/gky379	journal	May 2018
Htd2p/Yhr067p is a yeast 3-hydroxyacyl-ACP dehydratase essential for mitochondrial function and morphology Kastaniotis, Alexander J.; Autio, Kaija J.; Sormunen, Raija T. Molecular Microbiology, Vol. 53, Issue 5 https://doi.org/10.1111/j.1365-2958.2004.04191.x	journal	July 2004
The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols Fujita, Katsuhide; Matsuyama, Akinobu; Kobayashi, Yoshinori FEMS Yeast Research, Vol. 6, Issue 5 https://doi.org/10.1111/j.1567-1364.2006.00040.x	journal	August 2006
Introduction and expression of genes for metabolic engineering applications in Saccharomyces cerevisiae Da Silva, Nancy A.; Srikrishnan, Sneha FEMS Yeast Research, Vol. 12, Issue 2 https://doi.org/10.1111/j.1567-1364.2011.00769.x	journal	January 2012
Saccharomyces cerevisiae Genome-Wide Mutant Screen for Sensitivity to 2,4-Diacetylphloroglucinol, an Antibiotic Produced by Pseudomonas fluorescens Kwak, Youn-Sig; Han, Sangjo; Thomashow, Linda S. Applied and Environmental Microbiology, Vol. 77, Issue 5 https://doi.org/10.1128/AEM.02151-10	journal	March 2011
pdf1 , a Palmitoyl Protein Thioesterase 1 Ortholog in Schizosaccharomyces pombe : a Yeast Model of Infantile Batten Disease Cho, Steve K.; Hofmann, Sandra L. Eukaryotic Cell, Vol. 3, Issue 2 https://doi.org/10.1128/EC.3.2.302-310.2004	journal	April 2004
Lycopene overproduction in Saccharomyces cerevisiae through combining pathway engineering with host engineering Chen, Yan; Xiao, Wenhai; Wang, Ying Microbial Cell Factories, Vol. 15, Issue 1 https://doi.org/10.1186/s12934-016-0509-4	journal	June 2016
Translational landscape and protein biogenesis demands of the early secretory pathway in Komagataella phaffii Alva, Troy R.; Riera, Melanie; Chartron, Justin W. Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-020-01489-9	journal	January 2021
Quantitative CRISPR interference screens in yeast identify chemical-genetic interactions and new rules for guide RNA design Smith, Justin D.; Suresh, Sundari; Schlecht, Ulrich Genome Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s13059-016-0900-9	journal	March 2016
Modulation of acetate utilization in Komagataella phaffii by metabolic engineering of tolerance and metabolism Xu, Qin; Bai, Chenxiao; Liu, Yiqi Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1404-0	journal	March 2019
CRISPRi screens reveal genes modulating yeast growth in lignocellulose hydrolysate Gutmann, Friederike; Jann, Cosimo; Pereira, Filipa Biotechnology for Biofuels, Vol. 14, Issue 1 https://doi.org/10.1186/s13068-021-01880-7	journal	February 2021
Metabolic engineering of the oleaginous yeast Yarrowia lipolytica PO1f for production of erythritol from glycerol Jagtap, Sujit Sadashiv; Bedekar, Ashwini Ashok; Singh, Vijay Biotechnology for Biofuels, Vol. 14, Issue 1 https://doi.org/10.1186/s13068-021-02039-0	journal	September 2021
Metabolism of Hydrophobic Carbon Sources and Regulation of It inn-Alkane-Assimilating YeastYarrowia lipolytica Fukuda, Ryouichi Bioscience, Biotechnology, and Biochemistry, Vol. 77, Issue 6 https://doi.org/10.1271/bbb.130164	journal	June 2013
A Conserved Non-Canonical Docking Mechanism Regulates the Binding of Dual Specificity Phosphatases to Cell Integrity Mitogen-Activated Protein Kinases (MAPKs) in Budding and Fission Yeasts Sacristán-Reviriego, Almudena; Madrid, Marisa; Cansado, José PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0085390	journal	January 2014
RSC Chromatin-Remodeling Complex Is Important for Mitochondrial Function in Saccharomyces cerevisiae Imamura, Yuko; Yu, Feifei; Nakamura, Misaki PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0130397	journal	June 2015
Sequence Assembly of Yarrowia lipolytica Strain W29/CLIB89 Shows Transposable Element Diversity Magnan, Christophe; Yu, James; Chang, Ivan PLOS ONE, Vol. 11, Issue 9 https://doi.org/10.1371/journal.pone.0162363	journal	September 2016
Large‐scale image‐based profiling of single‐cell phenotypes in arrayed CRISPR‐Cas9 gene perturbation screens de Groot, Reinoud; Lüthi, Joel; Lindsay, Helen Molecular Systems Biology, Vol. 14, Issue 1 https://doi.org/10.15252/msb.20178064	journal	January 2018
The dual role of candida glabrata drug:H+ antiporter CgAqr1 (ORF CAGL0J09944g) in antifungal drug and acetic acid resistance Costa, Catarina; Henriques, André; Pires, Carla Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00170	journal	January 2013
Pexophagy: The Selective Autophagy of Peroxisomes Dunn, Jr., William A.; Cregg, James M.; Kiel, Jan A. K. W. Autophagy, Vol. 1, Issue 2 https://doi.org/10.4161/auto.1.2.1737	journal	July 2005
Systematic analysis of membrane contact sites in Saccharomyces cerevisiae uncovers modulators of cellular lipid distribution Castro, Inês Gomes; Shortill, Shawn P.; Dziurdzik, Samantha Katarzyna eLife https://doi.org/10.7554/eLife.74602	preprint	November 2022

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