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Exploitation of genus Rhodosporidium for microbial lipid production

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Abstract

Oleaginous microorganisms are receiving significant attention worldwide for their utility in biodiesel production and the potentiality to produce some specialty-type lipids. There is an increasing interest in isolation/adaption of robust microbe strains and design of innovative fermentation processes to make microbial lipid production a more efficient and economically feasible bio-process. Currently, the genus Rhodosporidium has been considered an important candidate, for the reason that several strains belonging to this genus have shown excellent capabilities of lipid accumulation, broad adaptabilities to various substrates, and co-production of some carotenoids. This paper reviews the current trends in the exploitation of Rhodosporidium species for microbial lipid production, including the utilization of various (single or mixed, pure or waste-derived) substrates, progress of genetic modification and metabolic engineering, innovations in fermentation mode, lipid characterizations and their potential applications. Finally, the constraints and perspectives of cultivating Rhodosporidium species for lipid production are also discussed.

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References

  • Abbott E, Ianiri G, Castoria R, Idnurm A (2013) Overcoming recalcitrant transformation and gene manipulation in Pucciniomycotina yeasts. Appl Microbiol Biotechnol 97:283–295

    Article  CAS  Google Scholar 

  • Bommareddy R, Sabra W, Maheshwari G, Zeng A (2015) Metabolic network analysis and experimental study of lipid production in Rhodosporidium toruloides grown on single and mixed substrates. Microb Cell Fact 14:36

    Article  Google Scholar 

  • Bommareddy R, Sabra W, Zeng A (2017) Glucose-mediated regulation of glycerol uptake in Rhodosporidium toruloides: Insights through transcriptomic analysis on dual substrate fermentation. Eng life Sci. doi:10.1002/elsc.201600010

    Google Scholar 

  • Chen Z, Liu P, Liu Y, Tang H, Chen Y, Zhang L (2014) Identification and characterization of a type-2 diacylglycerol acyltransferase (DGAT2) from Rhodosporidium diobovatum. Antonie Van Leeuwenhoek 106:1127–1137

    Article  CAS  Google Scholar 

  • Cui J, He S, Ji X, Lin L, Wei Y, Zhang Q (2016) Identification and characterization of a novel bifunctional Delta(12) Delta(15)-fatty acid desaturase gene from Rhodosporidium kratochvilovae. Biotechnol Lett 38:1155–1164

    Article  CAS  Google Scholar 

  • Davies R (1988) Yeast oil from cheese whey: process development. In: Moreton R (ed) Single cell oil. Longman Scientific & Technical, Harlow, pp 99–145

    Google Scholar 

  • Davies R, Holdsworth J (1992) Synthesis of lipids in yeasts: biochemistry, physiology and production. Adv Appl Lipid Res 1: 119–159

    CAS  Google Scholar 

  • Fei Q, O’Brien M, Nelson R, Chen X, Lowell A, Dowe N (2016) Enhanced lipid production by Rhodosporidium toruloides using different fed-batch feeding strategies with lignocellulosic hydrolysate as the sole carbon. Biotechnol Biofuels 9:130

    Article  Google Scholar 

  • Fillet S, Gibert J, Suarez B, Lara A, Ronchel C, Adrio J (2015) Fatty alcohols production by oleaginous yeast. J Ind Microbiol Biotechnol 42:1463–1472

    Article  CAS  Google Scholar 

  • Garay L, Sitepu I, Cajka T, Chandra I, Shi S, Lin T, German J, Fiehn O, Boundy-Mills K (2016) Eighteen new oleaginous yeast species. J Ind Microbiol Biotechnol 43:887–900

    Article  CAS  Google Scholar 

  • Gen Q, Wang Q, Chi Z (2014) Direct conversion of cassava starch into single cell oil by co-cultures of the oleaginous yeast. Renew Energy 62:522–526

    Article  Google Scholar 

  • Gierhart D (1984a) Multistage process for the preparation of fats and oils. US patent 4485172

  • Gierhart D (1984b) Preparation of fats and oils. US patent 4485173

  • Harde S, Wang Z, Horne M, Zhu J, Pan X (2016) Microbial lipid production from SPORL-pretreated Douglas fir by Mortierella isabellina. Fuel 175:64–74

    Article  CAS  Google Scholar 

  • Huang X, Liu J, Lu L, Peng K, Yang G, Liu J (2016) Culture strategies for lipid production using acetic acid as sole carbon source by Rhodosporidium toruloides. Bioresour Technol 206:141–149

    Article  CAS  Google Scholar 

  • Kiran E, Salakkam A, Trzcinski A, Bakir U, Webb C (2012) Enhancing the value of nitrogen from rapeseed meal for microbial oil production. Enzym Microb Technol 50:337–342

    Article  Google Scholar 

  • Kiran E, Trzcinski A, Webb C (2013) Microbial oil produced from biodiesel by-products could enhance overall production. Bioresour Technol 129:650–654

    Article  Google Scholar 

  • Koh C, Liu Y, Moehninsi, Du M, Ji L (2014) Molecular characterization of KU70 and KU80 homologues and exploitation of a KU70-deficient mutant for improving gene deletion frequency in Rhodosporidium toruloides. BMC Microbiol 14:50

    Article  Google Scholar 

  • Koutinas A, Chatzifragkou A, Kopsahelis N, Papanikolaou S, Kookos I (2014) Design and techno-economic evaluation of microbial oil production as a renewable resource for biodiesel and oleochemical production. Fuel 116:566–577

    Article  CAS  Google Scholar 

  • Kumar S, Kushwaha H, Bachhawat A, Raghava G, Ganesan K (2012) Genome Sequence of the Oleaginous Red Yeast Rhodosporidium toruloides MTCC 457. Eukaryot Cell 11:1083–1084

    Article  Google Scholar 

  • Lee J, Chen L, Shi J, Trzcinski A, Chen W (2014) Metabolomic profiling of Rhodosporidium toruloides grown on glycerol for carotenoid production during different growth phases. J Agric Food Chem 62:10203–10209

    Article  CAS  Google Scholar 

  • Lee J, Chen L, Cao B, Chen W (2016) Engineering Rhodosporidium toruloides with a membrane transporter facilitates production and separation of carotenoids and lipids in a bi-phasic culture. Appl Microbiol Biotechnol 100:869–877

    Article  CAS  Google Scholar 

  • Leiva-Candia D, Tsakona S, Kopsahelis N, Garcia I, Papanikolaou S, Dorado M, Koutinas A (2015) Biorefining of by-product streams from sunflower-based biodiesel production plants for integrated synthesis of microbial oil and value-added co-products. Bioresouc Technol 190: 57–65

    Article  CAS  Google Scholar 

  • Li Y, Zhao Z, Bai F (2007) High-density cultivation of oleaginous yeast Rhodosporidium toruloides Y4 in fed-batch culture. Enzym Microb Technol 41:312–317

    Article  Google Scholar 

  • Liang M, Jiang J (2013) Advancing oleaginous microorganisms to produce lipid via metabolic engineering technology. Prog Lipid Res 52:395–408

    Article  CAS  Google Scholar 

  • Lin X, Wang Y, Zhang S, Zhu Z, Zhou Y, Sun W, Wang X, Zhao Z (2014a) Functional integration of multiple genes into the genome of the oleaginous yeast Rhodosporidium toruloides. FEMS Yeast Res 14:547–555

    Article  CAS  Google Scholar 

  • Lin J, Li S, Sun M, Zhang C, Yang W, Zhang Z, Li X, Li S (2014b) Microbial lipid production by oleaginous yeast in D-xylose solution using a two-stage culture mode. RSC Adv 4:34944–34949

    Article  CAS  Google Scholar 

  • Ling J, Nip S, Shim H (2013) Enhancement of lipid productivity of Rhodosporidium toruloides in distillery wastewater by increasing cell density. Bioresour Technol 146:301–309

    Article  CAS  Google Scholar 

  • Ling J, Nip S, Cheok W, de Toledo R, Shim H (2014) Lipid production by a mixed culture of oleaginous yeast and microalga from distillery and domestic mixed wastewater. Bioresour Technol 173:132–139

    Article  CAS  Google Scholar 

  • Liu Y, Koh C, Sun L, Hlaing M, Du M, Peng N, Ji L (2013) Characterization of glyceraldehyde-3-phosphate dehydrogenase gene RtGPD1 and development of genetic transformation method by dominant selection in oleaginous yeast Rhodosporidium toruloides. Appl Microbiol Biotechnol 97:719–729

    Article  CAS  Google Scholar 

  • Liu Y, Koh C, Ngoh S, Ji L (2015) Engineering an efficient and tight d-amino acid-inducible gene expression system in Rhodosporidium Rhodotorula species. Microb Cell Fact 14:170

    Article  Google Scholar 

  • Liu Y, Zhang M, Wang T, Shi X, Li J, Jia L, Tang H, Zhang L (2016) Two acetyl-CoA synthetase isoenzymes are encoded by distinct genes in marine yeast Rhodosporidium diobovatum. Biotechnol Lett 38:417–423

    Article  CAS  Google Scholar 

  • Luque L, Orr V, Chen S, Westerhof R, Oudenhoven S, Rossum G, Kersten S, Berruti F, Rehmann L (2016) Lipid accumulation from pinewood pyrolysates by Rhodosporidium diobovatum and Chlorella vulgaris for biodiesel production. Bioresour Technol 214:660–669

    Article  CAS  Google Scholar 

  • Mannazzu I, Landolfo S, Silva T, Buzzini P (2015) Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest. World J Microbiol Biotechnol 31:1665–1673

    Article  CAS  Google Scholar 

  • Matsakas L, Bonturi N, Miranda E, Rova U, Christakopoulos P (2015) High concentrations of dried sorghum stalks as a biomass feedstock for single cell oil production by Rhodosporidium toruloides. Biotechnol Biofuels 8:6

    Article  Google Scholar 

  • Moreton R (1985) Modification of fatty acid composition of lipid accumulating yeasts with cyclopropene fatty acid desaturase inhibitors. Appl Microbiol Biotechnol 22:41–45

    Article  CAS  Google Scholar 

  • Moreton R, Clode D (1988) Microbial desaturase enzyme inhibitors and their use in a method of producing lipids. US patent 4778630

  • Morikawa Y, Zhao X, Liu D (2014) Biological co-production of ethanol and biodiesel from wheat straw- a case of dilute acid pretreatment. RSC Adv 4:37878–37888

    Article  CAS  Google Scholar 

  • Munch G, Sestric R, Sparling R, Levin D, Cicek N (2015) Lipid production in the under-characterized oleaginous yeasts Rhodosporidium babjevae and Rhodosporidium diobovatum from biodiesel-derived waste glycerol. Bioresour Technol 185:49–55

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2010) Yarrowia lipolytica: A model microorganism used for the production of tailor-made lipids. Eur J Lipid Sci Technol 112:639–654

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2011a) Lipids of oleaginous yeasts. Part Ι: Biochemistry of single cell oil production. Eur J Lipid Sci Technol 113:1031–1051

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2011b) Lipids of oleaginous yeasts. Part ΙΙ: technology and potential applications. Eur J Lipid Sci Technol 113:1052–1073

    Article  CAS  Google Scholar 

  • Parreira T, Freitas C, Reis A, Roseiro J, Silva T (2015) Carbon concentration and oxygen availability affect lipid and carotenoid production by carob pulp syrup. Eng. Life Sci 15:815–823

    Article  CAS  Google Scholar 

  • Patel A, Pravez M, Deeba F, Pruthi V, Singh R, Pruthi P (2014) Boosting accumulation of neutral lipids in Rhodosporidium kratochvilovae HIMPA1 grown on hemp seed. Bioresour Technol 165:214–222

    Article  CAS  Google Scholar 

  • Patel A, Pruthi V, Singh R, Pruthi P (2015a) Synergistic effect of fermentable and non-fermentable carbon sources enhances TAG accumulation in oleaginous yeast Rhodosporidium kratochvilovae HIMPA1. Bioresour Technol 188:136–144

    Article  CAS  Google Scholar 

  • Patel A, Sindhu D, Arora N, Singh R, Pruthi V, Pruthi P (2015b) Biodiesel production from non-edible lignocellulosic biomass of Cassia fistula L. fruit pulp using oleaginous yeast Rhodosporidium kratochvilovae HIMPA1. Bioresour Technol 197:91–98

    Article  CAS  Google Scholar 

  • Polburee P, Yongmanitchai W, Honda K, Ohashi T, Yoshida T, Fujiyama K, Limtong S (2016) Lipid production from biodiesel-derived crude glycerol by Rhodosporidium fluviale DMKU-RK253 using temperature shift with high cell density. Biochem Eng J 112:208–218

    Article  CAS  Google Scholar 

  • Qi F, Kitahara Y, Wang Z, Zhao X, Du W, Liu D (2014) Novel mutant strains of Rhodosporidium toruloides by plasma mutagenesis approach and their tolerance for inhibitors in lignocellulosic hydrolysate. J Chem Technol Biotechnol 89:735–742

    Article  CAS  Google Scholar 

  • Qi F, Zhao X, Kitahara Y, Li T, Ou X, Du W, Liu D, Huang J (2017) Integrative transcriptomic and proteomic analysis of the mutant lignocellulosic hydrolysate-tolerant Rhodosporidium toruloides. Eng. Life Sci. doi:10.1002/elsc.201500143

    Google Scholar 

  • Shi J, Feng H, Lee J, Chen W (2013) Comparative proteomics profile of lipid-cumulating oleaginous yeast: An iTRAQ-coupled 2-D LC-MS MS analysis. PloS ONE 8:e85532

    Article  Google Scholar 

  • Signori L, Ami D, Posteri R, Giuzzi A, Mereghetti P, Porro D, Branduardi P (2016) Assessing an effective feeding strategy to optimize crude glycerol utilization as sustainable carbon source for lipid accumulation in oleaginous yeasts. Microb Cell Fact 15:75

    Article  Google Scholar 

  • Tai M, Stephanopoulos G (2013) Engineering the push and pull of lipid biosynthesis in oleaginous yeast Yarrowia lipolytica for biofuel production. Metab Eng 15:1–9

    Article  CAS  Google Scholar 

  • Tchakouteu S, Kalantzi O, Gardeli C, Koutinas A, Aggelis G, Papanikolaou S (2015) Lipid production by yeasts growing on biodiesel-derived crude glycerol strain selection and impact of substrate concentration on the fermentation efficiency. J Appl Microbiol 118:911–927

    Article  CAS  Google Scholar 

  • Tchakouteu S, Kopsahelis N, Chatzifragkou A, Kalantzi O, Stoforos N, Koutinas A, Aggelis G, Papanikolaou S (2017) Rhodosporidium toruloides cultivated in NaCl-enriched glucose-based media: Adaptation dynamics and lipid production. Eng. Life Sci. doi:10.1002/elsc.201500125

    Google Scholar 

  • Tully M, Gilbert H (1985) Transformation of Rhodosporidium toruloides. Gene 36:235–240

    Article  CAS  Google Scholar 

  • Vieira J, Ienczak J, Rossell C, Pradella J, Franco T (2014) Microbial lipid production- screening with yeasts grown on Brazilian molasses. Biotechnol Lett 36:2433–2442

    Article  CAS  Google Scholar 

  • Wang Z, Fu W, Xu H, Chi Z (2014) Direct conversion of inulin into cell lipid by an inulinase-producing yeast Rhodosporidium toruloides 2F5. Bioresour Technol 161:131–136

    Article  CAS  Google Scholar 

  • Wang Y, Lin X, Zhang S, Sun W, Ma S, Zhao Z (2016) Cloning and evaluation of different constitutive promoters in the oleaginous yeast Rhodosporidium toruloides. Yeast 33:99–106

    Article  CAS  Google Scholar 

  • Wasylenko T, Ahn W, Stephanopoulos G (2015) The oxidative pentose phosphate pathway is the primary source of NADPH for lipid overproduction from glucose in Yarrowia lipolytica. Metab Eng 30:27–39

    Article  CAS  Google Scholar 

  • Wiebe M, Koivuranta K, Renttila M, Ruohonen L (2012) Lipid production in batch and fed-batch cultures of Rhodosporidium toruloides from 5 and 6 carbon carbohydrates. BMC Biotechnol 12:26

    Article  CAS  Google Scholar 

  • Wu S, Zhao X, Shen H, Wang Q, Zhao Z (2011) Microbial lipid production by Rhodosporidium toruloides under sulfate-limited conditions. Bioresour Technol 102:1803–1807

    Article  CAS  Google Scholar 

  • Xu J, Zhao X, Wang W, Du W, Liu D (2012) Microbial conversion of biodiesel byproduct glycerol to triacylglycerols by oleaginous yeast Rhodosporidium toruloides and the individual effect of some impurities on lipid production. Biochem Eng J 65:30–36

    Article  CAS  Google Scholar 

  • Xu J, Du W, Zhao X, Zhang G, Liu D (2013) Microbial oil production from various carbon sources and its use for biodiesel preparation. Biofuels Bioprod Biorefin 7:65–77

    Article  CAS  Google Scholar 

  • Xu P, Qiao K, Ahn W, Stephanopoulos G (2016) Engineering Yarrowia lipolytica as a platform for synthesis of drop-in transportation fuels and oleochemicals. Proc Natl Acad Sci 113:10848–10853

    Article  CAS  Google Scholar 

  • Xu J, Zhao X, Du W, Liu D (2017) Bioconversion of glycerol into lipids by Rhodosporidium toruloides in a two-stage process and characterization of lipid properties. Eng. Life Sci. doi:10.1002/elsc.201600062

    Google Scholar 

  • Yang F, Zhang S, Zhou Y, Zhu Z, Lin X, Zhao Z (2012) Characterization of the mitochondrial NAD(+)-dependent isocitrate dehydrogenase of the oleaginous yeast Rhodosporidium toruloides. Appl Microbiol Biotechnol 94:1095–1105

    Article  CAS  Google Scholar 

  • Yang X, Jin G, Gong Z, Shen H, Bai F, Zhao Z (2015) Recycling microbial lipid production wastes to cultivate oleaginous yeasts. Bioresour Technol 175:91–96

    Article  CAS  Google Scholar 

  • Zhang S, Ito M, Skerker J, Arkin A, Rao C (2016a) Metabolic engineering of the oleaginous yeast Rhodosporidium toruloides IFO0880 for lipid overproduction during high-density fermentation. Appl Microbiol Biotechnol 100:9393–9405

    Article  CAS  Google Scholar 

  • Zhang S, Skerker J, Rutter C, Maurer M, Arkin A, Rao C (2016b) Engineering Rhodosporidium toruloides for increased lipid production. Biotechnol Bioeng 113:1056–1066

    Article  CAS  Google Scholar 

  • Zhang X, Shen H, Yang X, Wang Q, Yu X, Zhao Z (2016c) Microbial lipid production by oleaginous yeasts on Laminaria residue hydrolysates. RSC Adv 6:26752–26756

    Article  CAS  Google Scholar 

  • Zhao X, Peng F, Du W, Liu C, Liu D (2012) Effects of some inhibitors on the growth and lipid accumulation of oleaginous yeast Rhodosporidium toruloides. Bioprocess Biosyst Eng 35:993–1004

    Article  CAS  Google Scholar 

  • Zhou W, Wang W, Li Y, Zhang Y (2013) Lipid production by Rhodosporidium toruloides Y2 in bioethanol wastewater and evaluation of biomass energetic yield. Bioresour Technol 127:435–440

    Article  CAS  Google Scholar 

  • Zhu Z, Zhang S, Liu H, Shen H, Lin X, Yang F, Zhou Y, Jin G, Ye M, Zou H, Zhao Z (2012) A multi-omic map of the lipid-producing yeast Rhodosporidium toruloides. Nat Commun 3:1112

    Article  Google Scholar 

  • Zhu Z, Ding Y, Gong Z, Yang L, Zhang S, Zhang C, Lin X, Shen H, Zou H, Xie Z, Yang F, Zhao X, Liu P, Zhao Z (2015) Dynamics of the Lipid Droplet Proteome of the Oleaginous Yeast Rhodosporidium toruloides. Eukaryot Cell 14:252–264

    Article  CAS  Google Scholar 

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Acknowledgements

The authors express their gratitude to the support from China Scholarship Council and Zhejiang Provincial Education Department Support Program (Y201533267).

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  1. Zhejiang Police College, Hangzhou, 310053, Zhejiang, People’s Republic of China

    Jingyang Xu

  2. Department of Chemical Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

    Jingyang Xu

  3. Department of Chemical Engineering, Institute of Applied Chemistry, Tsinghua University, Beijing, 100084, People’s Republic of China

    Dehua Liu

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Xu, J., Liu, D. Exploitation of genus Rhodosporidium for microbial lipid production. World J Microbiol Biotechnol 33, 54 (2017). https://doi.org/10.1007/s11274-017-2225-6

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