Yarrowia lipolytica Strains and Their Biotechnological Applications: How Natural Biodiversity and Metabolic Engineering Could Contribute to Cell Factories Improvement
Abstract
:1. Introduction
2. Everything You Always Wanted to Know about Yarrowia lipolytica (Briefly Resumed)
2.1. Natural Habitats and Safety
2.2. Main Characteristics
2.2.1. Physico-Chemical Conditions for Growth
2.2.2. Ploidy and Morphology
2.2.3. Carbon Sources
2.2.4. Secretion Pathway
2.2.5. Lipid Storage
2.2.6. Genomic Organization
2.3. An Impressive Curriculum Vitae: Short Review of Past, Present and Future Y. lipolytica Uses
2.3.1. Industrial Applications of Wild-Type or Traditionally Improved Strains
2.3.2. Commercial Applications of Genetically Modified Strains
2.3.3. Towards a Bio-Based Economy: Rewiring Strain Metabolism for Alternative Substrates
2.3.4. Potential Applications of Genetically Modified Strains: Bioproducts and Biofuels
2.3.5. Potential Applications of Genetically Modified Strains: Nanoparticles and Biomaterials
2.4. Long-Lost Relatives: Other Yeasts of the Yarrowia Clade
2.4.1. Brief Outline of Phylogeny, Habitat and Characteristics
2.4.2. Potential Applications of Other Yeasts of the Yarrowia Clade
3. Fantastic Yeasts and Where to Find Them: Yarrowia Strains and Yeast Collections
3.1. Oldies but Goodies: Elder Y. lipolytica Strains and Their Derivatives
3.1.1. From Paris Sewer to Worldwide Renown: The Success Story of W29
3.1.2. W29 and ATCC 18942 Progeny: E129 and E150 Strains
3.1.3. W29 Derivatives: The Po1 Series of Strains
3.1.4. Other Derivatives of W29: Obese Strains
3.1.5. Other Derivatives of W29: High-Throughput Expression Platforms for Protein Engineering
3.1.6. Other Derivatives of W29: Glyco-Engineered Strains for Producing Therapeutic Proteins
3.1.7. The Outsider H222
3.2. Gold Diggers: How to Find Nuggets in Old Mines
3.3. Finders Keepers: For a Good Isolate, Help Yourself
3.3.1. A-101 and Derivatives
3.3.2. ACA-DC 50109, Its Derivatives and Other Greek Y. lipolytica Isolates
3.3.3. New Kids on the Block: Y. lipolytica Strains Isolated or Noticed More Recently
4. A Brave New World of Engineered Strains: Tools and Strategies for Building Y. lipolytica Cell Factories
4.1. To Be or Not to Be Integrated: Types of Vectors and Assembly Methods
4.1.1. Episomal Vectors
4.1.2. Integrative Vectors and Cassettes
4.1.3. Multiple Transcription Unit Vectors, In Vitro DNA Assembly Methods and Y. lipolytica Toolboxes
4.1.4. In Vivo DNA Assembly Methods by Homologous Recombination and Artificial Chromosomes
4.2. Functional Elements for the Design of Expression Cassettes
4.2.1. Natural Y. lipolytica Promoters and Promoter Engineering
4.2.2. Natural and Synthetic Terminators
4.2.3. Targeting the Secretion Pathway: Secretion Signals and Surface Display Systems
4.2.4. Targeting Organelles for Subcellular Compartment Engineering
4.2.5. Selection Marker Genes and Marker Rescue Systems
4.3. Gene Editing and Whole Genome Analysis Technologies: CRISPR and Other Tools
4.3.1. CRISPR Tools and Y. lipolytica CRISPR-Cas9 Toolboxes for Gene Editing
4.3.2. TALEN Tools for Gene Editing in Y. lipolytica
4.3.3. Other CRISPR Tools for Base Editing and For Gene Repression or Activation
4.3.4. Transposomics and CRISPR-Derived Tools for Whole Genome Analysis in Y. lipolytica
4.4. How Gene Editing Can Leverage Strain Biodiversity and Be a Source of New Engineering Strategies
4.4.1. Increasing the Homologous Recombination Efficiency in Y. lipolytica
4.4.2. Diploid Strain Formation and Sexual Hybridization Following Mating Type Switching
4.5. Towards a Holistic View of Cell Factories and Bioprocesses Development
4.5.1. The Y. lipolytica Pan-Genome
4.5.2. Genome-Scale Omics Tools and Metabolic Models
4.5.3. Adaptative Evolution Strategies and Bioprocess Engineering
5. Conclusions in the Shape of a Question Mark: What Future for GMOs in Our Societies?
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
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Strain Usual Name/Origin (Reference Number in Yeast Collections—cf. Table 2) | Genotype Phenotype | Remarkable Characteristics | Usual Applications |
---|---|---|---|
A-101/carwash effluents, Poland [123] not publicly available (a) | ND wild-type prototroph | robust growth on oil [123], high citric acid production [124], sequenced strain [125] | in situ soil bioremediation [51,52], citric acid production [124], UV-mutagenesis and metabolic engineering host for design of improved strains producing citrate or erythritol [70,126,127,128] |
ACA-DC 50109 [aka LGAM S(7)1]/Greece [129] (b) | ND wild-type prototroph | very high lipid content and productivity [129,130], robust growth on crude glycerol, simultaneous high lipid and citric acid yields [131] | production of organic acids (notably citric acid) and SCO [129,130,131,132,133,134], including cocoa butter substitute [31,32], parent of evolved strain with increase oleaginicity [135], metabolic engineering host for design of improved GM strains [133,134] |
ACA-DC 5033 [aka ACA-YC 5033]/acid sourdough, Greece [136] | ND wild-type prototroph | robust growth on crude glycerol, simultaneous high lipid and citric acid yields [24] | SCO, citric acid and polyol production [24,137] |
ATCC 18942 [aka YB-423]/corn-processing plant, USA [138] (CBS 6124, CLIB 183, JCM 2320 and 8060, MUCL 29853, NBRC 1548, NRRL YB-423) | MatA MatB wild-type prototroph | diploid type strain [138], robust growth [139] | yeast biomass production [139] |
ATCC 20362 [aka 2002]/USA | ND wild-type prototroph | robust growth, high lipid content and productivity [57] | degradation of petroleum crude oil (US patent 3856667A), metabolic engineering host for design of Dupont GM PUFA-producing platform (cf. Section 2.3.2) [57,58] |
ATCC 48436/soil, Japan [140] (CBS 6303, CLIB 703, JCM 8054, NBRC 10073) | MatA wild-type prototroph | produces lipase activators [140] | lipase production [140], parent strain for Artechno highly lipolytic mutants used for bioremediation (cf. Section 2.3.1) |
D 1805/France [141] (ATCC 20390) | MatA MatB wild-type prototroph | non-sporulating diploid, robust growth [141,142], self-cycling fermentation [143] | organic acid production [143] |
H222/soil, Germany [10,144] (CLIB 80) | MatA wild-type prototroph | better fructose assimilation, high citric acid production [144], sequenced strain [34,37] | organic acid production, metabolic engineering host for design of improved GM strains [145,146] |
NCIM 3589/marine waters, India [147] | ND wild-type prototroph | biofilm formation [148] emulsifier production [149] | gold nanoparticle production [102] |
SWJ-1b/marine fish gut, China [4] (MCCC 2E00068) | ND wild-type prototroph | high level of crude protein [4] | citric acid and SCP production [150], metabolic engineering host for design of improved GM strains [151,152] ARTP-mutagenesis host for design of improved strains producing erythritol [153] |
W29/sewage water *, France [11,154] (ATCC 20460, CBS 7504, CICC 1778, CLIB 89, NBRC 113670, NRLL Y-3178, VKPM Y-3178) | MatA wild-type prototroph | high secretion level of proteins [10,155], sequenced strain [36,156] | organic acid production [11], basis for the Po1 series of heterologous protein-producing GM strains and the JMY2566 GM strain for high-throughput applications (cf. Figure 2), basis for GM obese strains (cf. Section 3.1.4) |
E129/GM from a W29 and ATCC 18942 crossing [10,157] (CLIB 121) (cf. Figure 2) | MatA, lys11-23, leu2-270, ura3-302, xpr2-322 Lys−, Leu−, Ura−, Suc+, ΔAEP | able to grow on sucrose [10,15] deleted for alkaline extracellular protease [10] | heterologous protein production [155] |
E150/GM from a W29 and ATCC 18942 crossing [10,157] (CLIB 122) (cf. Figure 2) | MatB, his1, leu2-270, ura3-302, xpr2-322 His−, Leu−, Ura−, Suc+, ΔAEP | able to grow on sucrose [10,15] deleted for alkaline extracellular protease [10], reference sequenced strain [33,34] | reference for assembling and annotating genomes [33,34] |
Po1d/GM from W29 [158] (CLIB 139) (cf. Figure 2) | MatA, leu2-270, ura3-302, xpr2-322 Leu−, Ura−, Suc+, ΔAEP | able to grow on sucrose [15] deleted for alkaline extracellular protease [158] | heterologous protein production [19,20,158], metabolic engineering host for design of GM strains for multiple applications [19,20] metabolic engineering host for design of Oxyrane ERT-producing platform (cf. Section 2.3.2) [61] |
Po1f/GM from W29 [159] (ATCC MYA-2613, CLIB 724, VKPM Y-3155) (cf. Figure 2) | MatA, leu2-270, ura3-302, xpr2-322, axp1-2 Leu−, Ura−, Suc+, ΔAEP, ΔAXP | able to grow on sucrose [15] deleted for both extracellular proteases [159], sequenced strain [160,161] | heterologous protein production [19,20,159], metabolic engineering host for design of GM strains for multiple applications [19,20] |
Po1g/GM from W29 [159] (CLIB 725) (cf. Figure 2) | MatA, leu2-270, ura3-302::URA3, xpr2-322, axp1-2 Leu−, Suc+, ΔAEP, ΔAXP | able to grow on sucrose [15] deleted for both extracellular proteases, carry a pBR322 docking platform [159] | heterologous protein production [19,20,159], included in the YLEX kit for expression/secretion of heterologous proteins [19,20] (cf. Section 2.3.2) |
Po1h/GM from W29 [18,43] (CLIB 882) (cf. Figure 2) | MatA, ura3-302, xpr2-322, axp1-2 Ura−, Suc+, ΔAEP, ΔAXP | able to grow on sucrose [15] deleted for both extracellular proteases [18,43] | heterologous protein production [18,19,20,43], metabolic engineering host for design of GM strains for multiple applications [19,20] |
Po1t/GM from W29 [18,43] (CLIB 883) (cf. Figure 2) | MatA, leu2-270, LEU2, ura3-302::URA3, xpr2-322, axp1-2 Suc+, ΔAEP, ΔAXP | able to grow on sucrose [15] deleted for both extracellular proteases, carry a pBR322 docking platform, GM prototroph [18,43] | negative control for heterologous protein production by other Po1 strains [18,43] |
JMY2566/GM from W29 [162] (CLIB 1779) (cf. Figure 2) | MatA, leu2-270, ura3::pTEF-RedStar2-LEU2-zeta, xpr2-322 Ura−, ΔAEP, RedStar2 | deleted for alkaline extracellular protease, fluorescent (red) strain, carry a zeta LTR sequences docking platform [162] | high-throughput mutant library screening [162] |
VKM Y-2373/Russia (Fed) VKM Y-2412/Russia (Fed) not publicly available (c) | ND wild-type prototroph | natural overproducers of, respectively, (iso)citric acid [163,164] and KGA [165] | organic acid production [163,164,165], basis for traditionally obtained 704-UV4-A/NG50 mutant for improved (iso)citric acid production [163] |
WSH-Z06/oil-polluted soil (refinery), China [166] not publicly available (d) | ND wild-type prototroph | thiamine-auxotrophic natural overproducer of KGA [166,167], sequenced strain [168] | KGA and keto acids production [167], basis for traditionally obtained hyper-producer mutants [168], metabolic engineering host for design of improved GM strains [169,170] |
YB-392/gluten settler, USA YB-419/maize fiber tailings, USA (NRRL YB-392 and NRRL YB-419) YB-420, YB-566 and YB-567 (not publicly available, do not appear on online catalog) | ND wild-type prototrophs | biomass hydrolysate consumption, inhibitor tolerance, high lipid/fatty acid or sugar alcohol production (cf. Section 3.2) [118], sequenced strains [171] | five strains selected as promising candidates for industrial biocatalysis [118,171] |
Country (Per Alphabetic Order) | Acronym of the Collection (WDCM Number) | Full Name of the Culture Collection | Website ISO Standard | Number of Strains of the Yarrowia Genus or Clade (C. for Candida) | Remarkable Yarrowia lipolytica Strains (Haploid, Unless Specified) |
---|---|---|---|---|---|
Belgium | BCCM/MUCL (WDCM 308) | Belgian Coordinated Collections of Microorganisms/MUCL Agro-food and Environmental Fungal Collection | http://bccm.belspo.be/about-us/bccm-mucl (accessed on 3 June 2021) ISO 9001:2015 | 29 Y. lipolytica + 3 C. (Y.) alimentaria 5 Y. deformans 1 C. (Y.) galli 1 C. hispaniensis 2 C. (Y.) hollandica 1 C. (Y.) osloensis * 4 Y. yakushimensis (including type strain for all) 2 Yarrowia sp. | MUCL 29853: diploid type strain (ATCC 18942) |
China (PR) | CICC (WDCM 582) | China Center of Industrial Culture Collection | http://www.china-cicc.org (accessed on 3 June 2021) http://www.english.china-cicc.org (accessed on 3 June 2021) ISO 9001:2008 ISO 17025:2016; ISO 17034:2018 | 34 Y. lipolytica (with intended biotechnological applications indicated) 1 Y. brassicae (type strain) | W29 (CICC 1778) CICC 33063 for erythritol production CICC 31268 and 32291 edible and feed yeasts |
CGMCC (WDCM 550) | China General Microbiological Culture Collection Center | http://www.cgmcc.net (accessed on 3 June 2021) http://www.cgmcc.net/english/ (accessed on 3 June 2021) ISO 9001:2010; ISO 14001:2010 | 113 Y. lipolytica | ||
MCCC (WDCM 1051) | Marine Culture Collection of China | http://www.mccc.org.cn/ (accessed on 3 June 2021) ISO 9001:2011 | 135 Y. lipolytica + 1 Yarrowia sp. | SWJ-1b (MCCC 2E00068): marine strain, for citric acid and SCP production | |
France | CIRM-Levures (WDCM 788) | Centre International de Ressources Microbiennes—Levures | https://www6.inrae.fr/cirm/Levures (accessed on 3 June 2021) https://www6.inrae.fr/cirm_eng/Yeasts (accessed on 3 June 2021) ISO 9001:2015 | 123 Y. lipolytica (including numerous GM laboratory strains) + 4 Y. deformans 1 C. hispaniensis (including type strain for both) 2 Yarrowia sp. | CLIB 183: diploid type strain (ATCC 18942) CLIB 703: type strain of Candida paralipolytica, for lipase production (ATCC 48436) E122 (CLIB 120): GM E129 (CLIB 121): GM E150 (CLIB 122): GM, sequenced (reference strain) H222 (CLIB 80): sequenced W29 (CLIB 89): sequenced W29 ura302 (CLIB 141): GM Po1a (CLIB 140): GM Po1d (CLIB 139): GM Po1e (CLIB 723): GM Po1f (CLIB 724): GM, sequenced Po1g (CLIB 725): GM Po1h (CLIB 882): GM Po1t (CLIB 883): GM |
Germany | DSMZ (WDCM 274) | Leibniz-Institut DSMZ-Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH | http://www.dsmz.de/ (accessed on 3 June 2021) ISO 9001:2008 ISO 17025:2005; ISO Guide 34:2009 | 6 Y. lipolytica + 1 Y. deformans | |
Greece | ACA-DC (WDCM 609) | Agricultural College of Athens-Dairy Collection | http://www.aca-dc.gr/ (accessed on 3 June 2021) | 16 Y. lipolytica (isolated mainly from food) | ACA-DC 50109 §, ACA-DC 5033: applied to citric acid and, respectively, SCO and polyol production |
India | NCIM (WDCM 3) | National Collection of Industrial Microorganisms | https://www.ncl-india.org/files/NCIM/Default.aspx (accessed on 3 June 2021) | 6 Y. lipolytica (erroneously indicated as Y. lipolitica) | NCIM 3589: marine strain, for gold nanoparticle production |
Japan | NBRC (WDCM 825) | NITE (National Institute of Technology and Evaluation) Biological Resource Center | https://www.nite.go.jp/en/nbrc/index.html (accessed on 3 June 2021) https://www.nite.go.jp/nbrc/catalogue/NBRCDispSearchServlet?lang=en (accessed on 3 June 2021) ISO 9001:2008 | 20 Y. lipolytica + 1 C. (Y.) phangngensis 1 Y. porcina (type strain for both) | NBRC 1548: diploid type strain (ATCC 18942) NBRC 10073: type strain of Candida paralipolytica, for lipase production (ATCC 48436) W29 (NBRC 113670) |
JCM (WDCM 567) | Japan Collection of Microorganisms | https://jcm.brc.riken.jp/en/ (accessed on 3 June 2021) ISO 9001:2015 | 22 Y. lipolytica + 4 Y. deformans 1 Y. keelungensis 1 Y. yakushimensis (including type strain for all) 5 Yarrowia sp. | JCM 8057: type strain (ATCC 20177) JCM 2320 and 8060: diploid type strain (ATCC 18942) JCM 8054: type strain of Candida paralipolytica, for lipase production (ATCC 48436) | |
Netherlands | CBS-KNAW (WDCM 133) | CBS Filamentous fungi and Yeast Collection-Westerdijk Fungal Biodiversity Institute | http://www.westerdijkinstitute.nl/ (accessed on 3 June 2021) https://wi.knaw.nl/page/Collection (accessed on 3 June 2021) https://theyeasts.org/ (accessed on 3 June 2021) ISO 9001:2007 | 38 Y. lipolytica + 3 C. (Y.) alimentaria 1 Y. brassicae 1 Y. bubula 18 Y. deformans 1 Y. divulgata 2 Y. galli 2 C. (Y.) hollandica 1 Y. keelungensis 4 Y. osloensis 1 Y. parophoni * 1 C. (Y.) phangngensis 2 Y. porcina 4 Y. yakushimensis 2 C. hispaniensis (including type strain for all) | CBS 8108: type strain (ATCC 20177) CBS 6124: diploid type strain (ATCC 18942) CBS 6303: type strain of Candida paralipolytica, for lipase production (ATCC 48436) W29 (CBS 7504) |
Russia (Fed) | VKPM (WDCM 588) | Russian National Collection of Industrial Microorganisms | https://vkpm.genetika.ru/ (accessed on 3 June 2021) | 28 Y. lipolytica | W29 (Y-3178) Po1f (Y-3155): GM Po1f Ura+ (Y-3483): GM |
VKM (WDCM 342) | All-Russian Collection of Microorganisms | http://www.vkm.ru/Catalogue.htm (accessed on 3 June 2021) | 17 Y. lipolytica + 1 Y. deformans (including type strain for all) | VKM Y-2373, VKM Y-2412: applied to organic acid production | |
USA | ATCC (WDCM 1) | American Type Culture Collection | http://www.atcc.org/ (accessed on 3 June 2021) ISO 9001:2015 ISO 13485:2016; ISO 17025:2017; ISO 17034:2016 | 132 Y. lipolytica + 1 Y. deformans 1 C. (Y.) phangngensis * (type strain for both) | ATCC 20177: type strain ATCC 18942: diploid type strain ATCC 48436: type strain of Candida paralipolytica, for lipase production D 1805 (ATCC 20390): non-sporulating diploid for organic acid production ATCC 20362: basis for Dupont PUFA-producing platform W29 (ATCC 20460) Po1f (ATCC MYA2613): GM |
NRRL (WDCM 97) | Agricultural Research Service (ARS) Culture Collection | http://nrrl.ncaur.usda.gov/ (accessed on 3 June 2021) | 34 Y. lipolytica + 1 C. (Y.) alimentaria 1 Y. bubula 2 Y. deformans 1 Y. divulgata 1 C. (Y.) galli 1 C. (Y.) hollandica 1 Y. keelungensis 1 C. (Y.) osloensis 2 C. (Y.) phangngensis * 1 Y. porcina 1 Y. yakushimensis 2 C. hispaniensis (including type strain for all) | NRRL YB-423: diploid type strain (ATCC 18942) YB-392, YB-419, YB-420, YB-566 and YB-567: selected as promising candidate strains for industrial biocatalysis, all sequenced W29 (Y-63746) |
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Madzak, C. Yarrowia lipolytica Strains and Their Biotechnological Applications: How Natural Biodiversity and Metabolic Engineering Could Contribute to Cell Factories Improvement. J. Fungi 2021, 7, 548. https://doi.org/10.3390/jof7070548
Madzak C. Yarrowia lipolytica Strains and Their Biotechnological Applications: How Natural Biodiversity and Metabolic Engineering Could Contribute to Cell Factories Improvement. Journal of Fungi. 2021; 7(7):548. https://doi.org/10.3390/jof7070548
Chicago/Turabian StyleMadzak, Catherine. 2021. "Yarrowia lipolytica Strains and Their Biotechnological Applications: How Natural Biodiversity and Metabolic Engineering Could Contribute to Cell Factories Improvement" Journal of Fungi 7, no. 7: 548. https://doi.org/10.3390/jof7070548