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Microbial conversion of xylose into useful bioproducts

Abstract

Microorganisms can produce a number of different bioproducts from the sugars in plant biomass. One challenge is devising processes that utilize all of the sugars in lignocellulosic hydrolysates. D-xylose is the second most abundant sugar in these hydrolysates. The microbial conversion of D-xylose to ethanol has been studied extensively; only recently, however, has conversion to bioproducts other than ethanol been explored. Moreover, in the case of yeast, D-xylose may provide a better feedstock for the production of bioproducts other than ethanol, because the relevant pathways are not subject to glucose-dependent repression. In this review, we discuss how different microorganisms are being used to produce novel bioproducts from D-xylose. We also discuss how D-xylose could be potentially used instead of glucose for the production of value-added bioproducts.

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References

  1. Agrawal M, Mao Z, Chen RR (2011) Adaptation yields a highly efficient xylose-fermenting Zymomonas mobilis strain. Biotechnol Bioeng 108(4):777–785. https://doi.org/10.1002/bit.23021

    CAS  Article  PubMed  Google Scholar 

  2. Albuquerque TL, da Silva IJ, de Macedo GR, Rocha MVP (2014) Biotechnological production of xylitol from lignocellulosic wastes: a review. Process Biochem 49(11):1779–1789. https://doi.org/10.1016/j.procbio.2014.07.010

    CAS  Article  Google Scholar 

  3. Alff-Tuomala S, Salusjarvi L, Barth D, Oja M, Penttila M, Pitkanen JP, Ruohonen L, Jouhten P (2016) Xylose-induced dynamic effects on metabolism and gene expression in engineered Saccharomyes cerevisiae in anaerobic glucose-xylose cultures. Appl Microbiol Biotechnol 100(2):969–985. https://doi.org/10.1007/s00253-015-7038-7

    CAS  Article  PubMed  Google Scholar 

  4. Alvarez HM (2006) Bacterial triacylglycerols. In: Welson LT (ed) Triglycerides and cholesterol research, vol 6. Nova Science, New York, pp 159–176

    Google Scholar 

  5. Baek S-H, Kwon EY, Kim YH, Hahn J-S (2016) Metabolic engineering and adaptive evolution for efficient production of D-lactic acid in Saccharomyes cerevisiae. Appl Microbiol Biotechnol 100(6):2737–2748. https://doi.org/10.1007/s00253-015-7174-0

    CAS  Article  PubMed  Google Scholar 

  6. Barbosa MF, de Medeiros MB, de Mancilha IM, Schneider H, Lee H (1988) Screening of yeasts for production of xylitol fromd-xylose and some factors which affect xylitol yield in Candida guilliermondii. J Ind Microbiol 3(4):241–251

    CAS  Article  Google Scholar 

  7. Beopoulos A, Verbeke J, Bordes F, Guicherd M, Bressy M, Marty A, Nicaud JM (2014) Metabolic engineering for ricinoleic acid production in the oleaginous yeast Yarrowia lipolytica. Appl Microbiol Biotechnol 98(1):251–262. https://doi.org/10.1007/s00253-013-5295-x

    CAS  Article  PubMed  Google Scholar 

  8. Bernard EM, Christiansen KJ, Tsang SF, Kiehn TE, Armstrong D (1981) Rate of arabinitol production by pathogenic yeast species. J Clin Microbiol 14(2):189–194

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Berovic M, Legisa M (2007) Citric acid production. Biotechnol Annu Rev 13:303–343

    CAS  Article  Google Scholar 

  10. Bisping B, Baumann U, Simmering R (1996) Effects of immobilization on polyol production by Pichia farinosa. Prog Biotechnol 11:395–401

    CAS  Article  Google Scholar 

  11. Blakley ER, Spencer JF (1962) Studies on the formation of D-arabitol by osmophilic yeasts. Can J Biochem Physiol 40:1737–1748

    CAS  Article  Google Scholar 

  12. Blazeck J, Hill A, Liu L, Knight R, Miller J, Pan A, Otoupal P, Alper HS (2014) Harnessing Yarrowia lipolytica lipogenesis to create a platform for lipid and biofuel production. Nat Commun 5:3131. https://doi.org/10.1038/ncomms4131

    CAS  Article  PubMed  Google Scholar 

  13. Blomberg A, Adler L (1992) Physiology of osmotolerance in fungi. Adv Microb Physiol 33:145–212

    CAS  Article  Google Scholar 

  14. Branduardi P, Sauer M, De Gioia L, Zampella G, Valli M, Mattanovich D, Porro D (2006) Lactate production yield from engineered yeasts is dependent from the host background, the lactate dehydrogenase source and the lactate export. Microb Cell Factories 5(1):4. https://doi.org/10.1186/1475-2859-5-4

    CAS  Article  Google Scholar 

  15. Brat D, Boles E (2013) Isobutanol production from D-xylose by recombinant Saccharomyes cerevisiae. FEMS Yeast Res 13(2):241–244. https://doi.org/10.1111/1567-1364.12028

    CAS  Article  PubMed  Google Scholar 

  16. Brat D, Boles E, Wiedemann B (2009) Functional expression of a bacterial xylose isomerase in Saccharomyes cerevisiae. Appl Environ Microbiol 75(8):2304–2311. https://doi.org/10.1128/aem.02522-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Brink DP, Borgström C, Tueros FG, Gorwa-Grauslund MF (2016) Real-time monitoring of the sugar sensing in Saccharomyes cerevisiae indicates endogenous mechanisms for xylose signaling. Microb Cell Factories 15(1):183. https://doi.org/10.1186/s12934-016-0580-x

    CAS  Article  Google Scholar 

  18. Bruinenberg PM, de Bot PHM, van Dijken JP, Scheffers WA (1984) NADH-linked aldose reductase: the key to anaerobic alcoholic fermentation of xylose by yeasts. Appl Microbiol Biotechnol 19(4):256–260. https://doi.org/10.1007/bf00251847

    CAS  Article  Google Scholar 

  19. Carly F, Fickers P (2018) Erythritol production by yeasts: a snapshot of current knowledge. Yeast 35(7):455–463

    CAS  Article  Google Scholar 

  20. Castro AR, Rocha I, Alves MM, Pereira MA (2016) Rhodococcus opacus B4: a promising bacterium for production of biofuels and biobased chemicals. AMB Express 6(1):35. https://doi.org/10.1186/s13568-016-0207-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Celińska E, Grajek W (2009) Biotechnological production of 2,3-butanediol—current state and prospects. Biotechnol Adv 27(6):715–725. https://doi.org/10.1016/j.biotechadv.2009.05.002

    CAS  Article  PubMed  Google Scholar 

  22. Chang MC, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2(12):674–681. https://doi.org/10.1038/nchembio836

    CAS  Article  PubMed  Google Scholar 

  23. Chatzifragkou A, Fakas S, Galiotou-Panayotou M, Komaitis M, Aggelis G, Papanikolaou S (2010) Commercial sugars as substrates for lipid accumulation in Cunninghamella echinulata and Mortierella isabellina fungi. Eur J Lipid Sci Technol 112(9):1048–1057

    CAS  Article  Google Scholar 

  24. Chen X, Nielsen KF, Borodina I, Kielland-Brandt MC, Karhumaa K (2011) Increased isobutanol production in Saccharomyes cerevisiae by overexpression of genes in valine metabolism. Biotechnol Biofuels 4:21. https://doi.org/10.1186/1754-6834-4-21

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Chung Y-S, Kim M-D, Lee W-J, Ryu Y-W, Kim J-H, Seo J-H (2002) Stable expression of xylose reductase gene enhances xylitol production in recombinant Saccharomyes cerevisiae. Enzym Microb Technol 30(6):809–816

    CAS  Article  Google Scholar 

  26. Cirino PC, Chin JW, Ingram LO (2006) Engineering Escherichia coli for xylitol production from glucose-xylose mixtures. Biotechnol Bioeng 95(6):1167–1176

    CAS  Article  Google Scholar 

  27. Colombié S, Dequin S, Sablayrolles JM (2003) Control of lactate production by Saccharomyes cerevisiae expressing a bacterial LDH gene. Enzym Microb Technol 33(1):38–46. https://doi.org/10.1016/S0141-0229(03)00082-6

    CAS  Article  Google Scholar 

  28. Dahiya JS (1991) Xylitol production by Petromyces albertensis grown on medium containing D-xylose. Can J Microbiol 37(1):14–18. https://doi.org/10.1139/m91-003

    CAS  Article  Google Scholar 

  29. Dequin S, Barre P (1994) Mixed lactic acid–alcoholic fermentation by Saccharomyes cerevisiae expressing the lactobacillus casei L(+)–LDH. Nat Biotechnol 12:173–177. https://doi.org/10.1038/nbt0294-173

    CAS  Article  Google Scholar 

  30. DeRisi JL, Iyer VR, Brown PO (1997) Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 278(5338):680–686

    CAS  Article  Google Scholar 

  31. Dey P, Banerjee J, Maiti MK (2011) Comparative lipid profiling of two endophytic fungal isolates—Colletotrichum sp. and Alternaria sp. having potential utilities as biodiesel feedstock. Bioresour Technol 102(10):5815–5823

    CAS  Article  Google Scholar 

  32. Dhiman SS, Jagtap SS, Jeya M, Haw J-R, Kang YC, Lee J-K (2012) Immobilization of Pholiota adiposa xylanase onto SiO2 nanoparticles and its application for production of xylooligosaccharides. Biotechnol Lett 34(7):1307–1313. https://doi.org/10.1007/s10529-012-0902-y

    CAS  Article  PubMed  Google Scholar 

  33. Dhiman SS, Kalyani D, Jagtap SS, Haw J-R, Kang YC, Lee J-K (2013) Characterization of a novel xylanase from Armillaria gemina and its immobilization onto SiO2 nanoparticles. Appl Microbiol Biotechnol 97(3):1081–1091. https://doi.org/10.1007/s00253-012-4381-9

    CAS  Article  PubMed  Google Scholar 

  34. Díaz T, Fillet S, Campoy S, Vázquez R, Viña J, Murillo J, Adrio JL (2018) Combining evolutionary and metabolic engineering in Rhodosporidium toruloides for lipid production with non-detoxified wheat straw hydrolysates. Appl Microbiol Biotechnol 102(7):3287–3300. https://doi.org/10.1007/s00253-018-8810-2

    CAS  Article  PubMed  Google Scholar 

  35. Díaz-Fernández D, Lozano-Martínez P, Buey RM, Revuelta JL, Jiménez A (2017) Utilization of xylose by engineered strains of Ashbya gossypii for the production of microbial oils. Biotechnol Biofuels 10(1):3. https://doi.org/10.1186/s13068-016-0685-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Dijken J, Scheffers A (1986) Redox balances in the metabolism of sugars by yeasts. FEMS Microbiol Rev 1(3–4):199–224

    Article  Google Scholar 

  37. Dunn KL, Rao CV (2014) Expression of a xylose-specific transporter improves ethanol production by metabolically engineered Zymomonas mobilis. Appl Microbiol Biotechnol 98(15):6897–6905. https://doi.org/10.1007/s00253-014-5812-6

    CAS  Article  PubMed  Google Scholar 

  38. Dunn KL, Rao CV (2015) High-throughput sequencing reveals adaptation-induced mutations in pentose-fermenting strains of Zymomonas mobilis. Biotechnol Bioeng 112(11):2228–2240. https://doi.org/10.1002/bit.25631

    CAS  Article  PubMed  Google Scholar 

  39. Egner A, Jakobs S, Hell SW (2002) Fast 100-nm resolution three-dimensional microscope reveals structural plasticity of mitochondria in live yeast. Proc Natl Acad Sci U S A 99(6):3370–3375. https://doi.org/10.1073/pnas.052545099

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Escalante J, Caminal G, Figueredo M, de Mas C (1990) Production of arabitol from glucose by Hansenula polymorpha. J Ferment Bioeng 70(4):228–231. https://doi.org/10.1016/0922-338X(90)90053-Y

    CAS  Article  Google Scholar 

  41. Fakas S, Papanikolaou S, Batsos A, Galiotou-Panayotou M, Mallouchos A, Aggelis G (2009) Evaluating renewable carbon sources as substrates for single cell oil production by Cunninghamella echinulata and Mortierella isabellina. Biomass Bioenergy 33(4):573–580

    CAS  Article  Google Scholar 

  42. Falony G, Honkala S, Runnel R, Olak J, Nõmmela R, Russak S, Saag M, Mäkinen P-L, Mäkinen K, Vahlberg T (2016) Long-term effect of erythritol on dental caries development during childhood: a posttreatment survival analysis. Caries Res 50(6):579–588

    CAS  Article  Google Scholar 

  43. Farwick A, Bruder S, Schadeweg V, Oreb M, Boles E (2014) Engineering of yeast hexose transporters to transport d-xylose without inhibition by d-glucose. Proc Natl Acad Sci U S A 111(14):5159–5164. https://doi.org/10.1073/pnas.1323464111

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Felpeto-Santero C, Rojas A, Tortajada M, Galán B, Ramón D, García JL (2015) Engineering alternative isobutanol production platforms. AMB Express 5:32. https://doi.org/10.1186/s13568-015-0119-2

    CAS  Article  PubMed Central  Google Scholar 

  45. Feng X, Lian J, Zhao H (2015) Metabolic engineering of Saccharomyes cerevisiae to improve 1-hexadecanol production. Metab Eng 27:10–19. https://doi.org/10.1016/j.ymben.2014.10.001

    CAS  Article  PubMed  Google Scholar 

  46. Ferreira R, Teixeira PG, Siewers V, Nielsen J (2018) Redirection of lipid flux toward phospholipids in yeast increases fatty acid turnover and secretion. Proc Natl Acad Sci U S A 115:1262–1267. https://doi.org/10.1073/pnas.1715282115

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Gancedo JM (1998) Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62(2):334–361

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Gao D, Zeng J, Zheng Y, Yu X, Chen S (2013) Microbial lipid production from xylose by Mortierella isabellina. Bioresour Technol 133:315–321. https://doi.org/10.1016/j.biortech.2013.01.132

    CAS  Article  PubMed  Google Scholar 

  49. Gárdonyi M, Hahn-Hägerdal B (2003) The Streptomyces rubiginosus xylose isomerase is misfolded when expressed in Saccharomyes cerevisiae. Enzym Microb Technol 32(2):252–259. https://doi.org/10.1016/S0141-0229(02)00285-5

    Article  Google Scholar 

  50. Gong C-S, Chen LF, Tsao GT (1981) Quantitative production of xylitol from D-xylose by a high-xylitol producing yeast mutant Candida tropicalis HXP2. Biotechnol Lett 3(3):125–130. https://doi.org/10.1007/bf00127364

    CAS  Article  Google Scholar 

  51. Görke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624. https://doi.org/10.1038/nrmicro1932

    CAS  Article  PubMed  Google Scholar 

  52. Guo J, Li J, Chen Y, Guo X, Xiao D (2016a) Improving erythritol production of Aureobasidium pullulans from xylose by mutagenesis and medium optimization. Appl Biochem Biotechnol 180(4):717–727. https://doi.org/10.1007/s12010-016-2127-3

    CAS  Article  PubMed  Google Scholar 

  53. Guo W, Sheng J, Zhao H, Feng X (2016b) Metabolic engineering of Saccharomyes cerevisiae to produce 1-hexadecanol from xylose. Microb Cell Factories 15:24. https://doi.org/10.1186/s12934-016-0423-9

    CAS  Article  Google Scholar 

  54. Häcker B, Habenicht A, Kiess M, Mattes R (1999) Xylose utilisation: cloning and characterisation of the xylose reductase from Candida tenuis. Biol Chem 380(12):1395–1403

    Article  Google Scholar 

  55. Hahn-Hagerdal B, Karhumaa K, Fonseca C, Spencer-Martins I, Gorwa-Grauslund MF (2007a) Towards industrial pentose-fermenting yeast strains. Appl Microbiol Biotechnol 74(5):937–953. https://doi.org/10.1007/s00253-006-0827-2

    CAS  Article  PubMed  Google Scholar 

  56. Hahn-Hagerdal B, Karhumaa K, Jeppsson M, Gorwa-Grauslund MF (2007b) Metabolic engineering for pentose utilization in Saccharomyes cerevisiae. Adv Biochem Eng Biotechnol 108:147–177. https://doi.org/10.1007/10_2007_062

    CAS  Article  PubMed  Google Scholar 

  57. Hajny GJ (1964) D-arabitol production by Endomycopsis chodati. Appl Environ Microbiol 12(1):87–92

    CAS  Google Scholar 

  58. Hamacher T, Becker J, Gardonyi M, Hahn-Hägerdal B, Boles E (2002) Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiol 148(9):2783–2788

    CAS  Article  Google Scholar 

  59. Harhangi HR, Akhmanova AS, Emmens R, van der Drift C, de Laat WTAM, van Dijken JP, Jetten MSM, Pronk JT, Op den Camp HJM (2003) Xylose metabolism in the anaerobic fungus Piromyces sp. strain E2 follows the bacterial pathway. Arch Microbiol 180(2):134–141. https://doi.org/10.1007/s00203-003-0565-0

    CAS  Article  PubMed  Google Scholar 

  60. Hernández MA, Mohn WW, Martínez E, Rost E, Alvarez AF, Alvarez HM (2008) Biosynthesis of storage compounds by Rhodococcus jostii RHA1 and global identification of genes involved in their metabolism. BMC Genomics 9(1):600. https://doi.org/10.1186/1471-2164-9-600

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Hiele M, Ghoos Y, Rutgeerts P, Vantrappen G (1993) Metabolism of erythritol in humans: comparison with glucose and lactitol. Br J Nutr 69(1):169–176

    CAS  Article  Google Scholar 

  62. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315(5813):804–807. https://doi.org/10.1126/science.1137016

    CAS  Article  PubMed  Google Scholar 

  63. Hong Y, Dashtban M, Kepka G, Chen S, Qin W (2014) Overexpression of d-xylose reductase (xyl1) gene and antisense inhibition of d-xylulokinase (xyiH) gene increase xylitol production in Trichoderma reesei. Biomed Res Int 2014:8–8. https://doi.org/10.1155/2014/169705

    CAS  Article  Google Scholar 

  64. Huang C, X-f C, Xiong L, Ma L-l, Chen Y (2013) Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv 31(2):129–139

    CAS  Article  Google Scholar 

  65. Ingram-Smith C, Martin SR, Smith KS (2006) Acetate kinase: not just a bacterial enzyme. Trends Microbiol 14(6):249–253. https://doi.org/10.1016/j.tim.2006.04.001

    CAS  Article  PubMed  Google Scholar 

  66. Ishida N, Saitoh S, Tokuhiro K, Nagamori E, Matsuyama T, Kitamoto K, Takahashi H (2005) Efficient production of L-lactic acid by metabolically engineered Saccharomyes cerevisiae with a genome-integrated L-lactate dehydrogenase gene. Appl Environ Microbiol 71(4):1964–1970. https://doi.org/10.1128/aem.71.4.1964-1970.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  67. Isikgor FH, Becer CR (2015) Lignocellulosic biomass: a sustainable platform for the production of bio-based chemicals and polymers. Polym Chem 6(25):4497–4559. https://doi.org/10.1039/C5PY00263J

    CAS  Article  Google Scholar 

  68. Jagtap SS, Rao CV (2018) Production of D-arabitol from D-xylose by the oleaginous yeast Rhodosporidium toruloides IFO0880. Appl Microbiol Biotechnol 102(1):143–151. https://doi.org/10.1007/s00253-017-8581-1

    CAS  Article  PubMed  Google Scholar 

  69. Jagtap SS, Dhiman SS, Jeya M, Kang YC, Choi J-H, Lee J-K (2012) Saccharification of poplar biomass by using lignocellulases from Pholiota adiposa. Bioresour Technol 120:264–272. https://doi.org/10.1016/j.biortech.2012.06.002

    CAS  Article  PubMed  Google Scholar 

  70. Jagtap SS, Dhiman SS, Kim T-S, Li J, Lee J-K, Kang YC (2013) Enzymatic hydrolysis of aspen biomass into fermentable sugars by using lignocellulases from Armillaria gemina. Bioresour Technol 133:307–314. https://doi.org/10.1016/j.biortech.2013.01.118

    CAS  Article  PubMed  Google Scholar 

  71. Jagtap SS, Dhiman SS, Kim T-S, Kim I-W, Lee J-K (2014a) Characterization of a novel endo-β-1,4-glucanase from Armillaria gemina and its application in biomass hydrolysis. Appl Microbiol Biotechnol 98(2):661–669. https://doi.org/10.1007/s00253-013-4894-x

    CAS  Article  PubMed  Google Scholar 

  72. Jagtap SS, Woo SM, Kim T-S, Dhiman SS, Kim D, Lee J-K (2014b) Phytoremediation of diesel-contaminated soil and saccharification of the resulting biomass. Fuel 116:292–298. https://doi.org/10.1016/j.fuel.2013.08.017

    CAS  Article  Google Scholar 

  73. Janek T, Dobrowolski A, Biegalska A, Mirończuk AM (2017) Characterization of erythrose reductase from Yarrowia lipolytica and its influence on erythritol synthesis. Microb Cell Factories 16(1):118

    Article  Google Scholar 

  74. Jeffries TW (1983) Utilization of xylose by bacteria, yeasts, and fungi. In: Chan YK, Fiechter A, Gong C-S, Jansen NB, Janshekar H, Jeffries TW, Kurtzman CP, Maleszka R, McCracken LD, Neirinck L, Schneider H, Szczesny T, Tsao GT, Veliky IA, Volesky B, Wang PY (eds) Pentoses and lignin. Springer, Berlin, pp 1–32

    Google Scholar 

  75. Jeffries TW (2006) Engineering yeasts for xylose metabolism. Curr Opin Biotechnol 17(3):320–326. https://doi.org/10.1016/j.copbio.2006.05.008

    CAS  Article  PubMed  Google Scholar 

  76. Jeffries TW, Shi N-Q (1999) Genetic engineering for improved xylose fermentation by yeasts. In: Tsao GT, Brainard AP, Bungay HR, Cao NJ, Cen P, Chen Z, Du J, Foody B, Gong CS, Hall P, Ho NWY, Irwin DC, Iyer P, Jeffries TW, Ladisch CM, Ladisch MR, Lee YY, Mosier NS, Mühlemann HM, Sedlak M, Shi NQ, Tsao GT, Tolan JS, Torget RW, Wilson DB, Xia L (eds) Recent progress in bioconversion of lignocellulosics. Springer, Berlin, pp 117–161

    Chapter  Google Scholar 

  77. Jeffries TW, Grigoriev IV, Grimwood J, Laplaza JM, Aerts A, Salamov A, Schmutz J, Lindquist E, Dehal P, Shapiro H, Jin YS, Passoth V, Richardson PM (2007) Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis. Nat Biotechnol 25(3):319–326. https://doi.org/10.1038/nbt1290

    CAS  Article  PubMed  Google Scholar 

  78. Jeon YJ, Svenson CJ, Rogers PL (2005) Over-expression of xylulokinase in a xylose-metabolising recombinant strain of Zymomonas mobilis. FEMS Microbiol Lett 244(1):85–92. https://doi.org/10.1016/j.femsle.2005.01.025

    CAS  Article  PubMed  Google Scholar 

  79. Jeon WY, Yoon BH, Ko BS, Shim WY, Kim JH (2012) Xylitol production is increased by expression of codon-optimized Neurospora crassa xylose reductase gene in Candida tropicalis. Bioprocess Biosyst Eng 35(1–2):191–198

    CAS  Article  Google Scholar 

  80. Jeon WY, Shim WY, Lee SH, Choi JH, Kim JH (2013) Effect of heterologous xylose transporter expression in Candida tropicalis on xylitol production rate. Bioprocess Biosyst Eng 36(6):809–817

    CAS  Article  Google Scholar 

  81. Jeppsson M, Bengtsson O, Franke K, Lee H, Hahn-Hägerdal B, Gorwa-Grauslund MF (2006) The expression of a Pichia stipitis xylose reductase mutant with higher KM for NADPH increases ethanol production from xylose in recombinant Saccharomyes cerevisiae. Biotechnol Bioeng 93(4):665–673. https://doi.org/10.1002/bit.20737

    CAS  Article  PubMed  Google Scholar 

  82. Jin YS, Jones S, Shi NQ, Jeffries TW (2002) Molecular cloning of XYL3 (D-xylulokinase) from Pichia stipitis and characterization of its physiological function. Appl Environ Microbiol 68(3):1232–1239

    CAS  Article  Google Scholar 

  83. Jin YS, Laplaza JM, Jeffries TW (2004) Saccharomyes cerevisiae engineered for xylose metabolism exhibits a respiratory response. Appl Environ Microbiol 70(11):6816–6825. https://doi.org/10.1128/aem.70.11.6816-6825.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  84. Jin M, Slininger PJ, Dien BS, Waghmode S, Moser BR, Orjuela A, Sousa Lda C, Balan V (2015) Microbial lipid-based lignocellulosic biorefinery: feasibility and challenges. Trends Biotechnol 33(1):43–54. https://doi.org/10.1016/j.tibtech.2014.11.005

    CAS  Article  PubMed  Google Scholar 

  85. Johnsen U, Dambeck M, Zaiss H, Fuhrer T, Soppa J, Sauer U, Schonheit P (2009) D-xylose degradation pathway in the halophilic archaeon Haloferax volcanii. J Biol Chem 284(40):27290–27303. https://doi.org/10.1074/jbc.M109.003814

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  86. Jordan DB, Bowman MJ, Braker JD, Dien BS, Hector RE, Lee CC, Mertens JA, Wagschal K (2012) Plant cell walls to ethanol. Biochem J 442(2):241–252. https://doi.org/10.1042/bj20111922

    CAS  Article  PubMed  Google Scholar 

  87. Jordan P, Choe JY, Boles E, Oreb M (2016) Hxt13, Hxt15, Hxt16 and Hxt17 from Saccharomyes cerevisiae represent a novel type of polyol transporters. Sci Rep 6:23502. https://doi.org/10.1038/srep23502

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. Jovanović B, Mach RL, Mach-Aigner AR (2014) Erythritol production on wheat straw using Trichoderma reesei. AMB Express 4:34–34. https://doi.org/10.1186/s13568-014-0034-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  89. Kim S, Hahn J-S (2015) Efficient production of 2,3-butanediol in Saccharomyes cerevisiae by eliminating ethanol and glycerol production and redox rebalancing. Metab Eng 31:94–101. https://doi.org/10.1016/j.ymben.2015.07.006

    CAS  Article  PubMed  Google Scholar 

  90. Kim T-B, Lee Y-J, Kim P, Kim CS, Oh D-K (2004) Increased xylitol production rate during long-term cell recycle fermentation of Candida tropicalis. Biotechnol Lett 26(8):623–627

    CAS  Article  Google Scholar 

  91. Kim S-H, Yun J-Y, Kim S-G, Seo J-H, Park J-B (2010) Production of xylitol from D-xylose and glucose with recombinant Corynebacterium glutamicum. Enzym Microb Technol 46(5):366–371

    CAS  Article  Google Scholar 

  92. Kim SR, Ha S-J, Wei N, Oh EJ, Jin Y-S (2012) Simultaneous co-fermentation of mixed sugars: a promising strategy for producing cellulosic ethanol. Trends Biotechnol 30(5):274–282. https://doi.org/10.1016/j.tibtech.2012.01.005

    CAS  Article  PubMed  Google Scholar 

  93. Kim S-J, Seo S-O, Jin Y-S, Seo J-H (2013) Production of 2,3-butanediol by engineered Saccharomyes cerevisiae. Bioresour Technol 146:274–281. https://doi.org/10.1016/j.biortech.2013.07.081

    CAS  Article  PubMed  Google Scholar 

  94. Kim SJ, Seo SO, Park YC, Jin YS, Seo JH (2014) Production of 2,3-butanediol from xylose by engineered Saccharomyes cerevisiae. J Biotechnol 192(Pt B):376–382. https://doi.org/10.1016/j.jbiotec.2013.12.017

    CAS  Article  PubMed  Google Scholar 

  95. Kim S-J, Kim J-W, Lee Y-G, Park Y-C, Seo J-H (2017a) Metabolic engineering of Saccharomyes cerevisiae for 2,3-butanediol production. Appl Microbiol Biotechnol 101(6):2241–2250. https://doi.org/10.1007/s00253-017-8172-1

    CAS  Article  PubMed  Google Scholar 

  96. Kim S-J, Sim H-J, Kim J-W, Lee Y-G, Park Y-C, Seo J-H (2017b) Enhanced production of 2,3-butanediol from xylose by combinatorial engineering of xylose metabolic pathway and cofactor regeneration in pyruvate decarboxylase-deficient Saccharomyes cerevisiae. Bioresour Technol 245(Part B):1551–1557. https://doi.org/10.1016/j.biortech.2017.06.034

    CAS  Article  PubMed  Google Scholar 

  97. Kobayashi Y, Yoshida J, Iwata H, Koyama Y, Kato J, Ogihara J, Kasumi T (2013) Gene expression and function involved in polyol biosynthesis of Trichosporonoides megachiliensis under hyper-osmotic stress. J Biosci Bioeng 115(6):645–650

    CAS  Article  Google Scholar 

  98. Kosa M, Ragauskas AJ (2011) Lipids from heterotrophic microbes: advances in metabolism research. Trends Biotechnol 29(2):53–61

    CAS  Article  Google Scholar 

  99. Kotter P, Amore R, Hollenberg CP, Ciriacy M (1990) Isolation and characterization of the Pichia stipitis xylitol dehydrogenase gene, XYL2, and construction of a xylose-utilizing Saccharomyes cerevisiae transformant. Curr Genet 18(6):493–500

    CAS  Article  Google Scholar 

  100. Kurosawa K, Wewetzer SJ, Sinskey AJ (2013) Engineering xylose metabolism in triacylglycerol-producing Rhodococcus opacus for lignocellulosic fuel production. Biotechnol Biofuels 6(1):134. https://doi.org/10.1186/1754-6834-6-134

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  101. Kwak S, Jin YS (2017) Production of fuels and chemicals from xylose by engineered Saccharomyes cerevisiae: a review and perspective. Microb Cell Factories 16(1):82. https://doi.org/10.1186/s12934-017-0694-9

    Article  Google Scholar 

  102. Kwak S, Kim SR, Xu H, Zhang GC, Lane S, Kim H, Jin YS (2017) Enhanced isoprenoid production from xylose by engineered Saccharomyes cerevisiae. Biotechnol Bioeng 114(11):2581–2591. https://doi.org/10.1002/bit.26369

    CAS  Article  PubMed  Google Scholar 

  103. Kwon SG, Park SW, Oh DK (2006) Increase of xylitol productivity by cell-recycle fermentation of Candida tropicalis using submerged membrane bioreactor. J Biosci Bioeng 101(1):13–18. https://doi.org/10.1263/jbb.101.13

    CAS  Article  PubMed  Google Scholar 

  104. Lajoie CA, Kitner JB, Potochnik SJ, Townsend JM, Beatty CC, Kelly CJ (2016) Cloning, expression and characterization of xylose isomerase from the marine bacterium Fulvimarina pelagi in Escherichia coli. Biotechnol Prog 32(5):1230–1237. https://doi.org/10.1002/btpr.2309

    CAS  Article  PubMed  Google Scholar 

  105. Lane S, Dong J, Jin Y-S (2018) Value-added biotransformation of cellulosic sugars by engineered Saccharomyes cerevisiae. Bioresour Technol 260:380–394. https://doi.org/10.1016/j.biortech.2018.04.013

    CAS  Article  PubMed  Google Scholar 

  106. Lange N, Steinbuchel A (2011) Beta-carotene production by Saccharomyes cerevisiae with regard to plasmid stability and culture media. Appl Microbiol Biotechnol 91(6):1611–1622. https://doi.org/10.1007/s00253-011-3315-2

    CAS  Article  PubMed  Google Scholar 

  107. Lazar Z, Walczak E, Robak M (2011) Simultaneous production of citric acid and invertase by Yarrowia lipolytica SUC+ transformants. Bioresour Technol 102(13):6982–6989. https://doi.org/10.1016/j.biortech.2011.04.032

    CAS  Article  PubMed  Google Scholar 

  108. Lazar Z, Dulermo T, Neuvéglise C, Crutz-Le Coq A-M, Nicaud J-M (2014) Hexokinase—a limiting factor in lipid production from fructose in Yarrowia lipolytica. Metab Eng 26:89–99. https://doi.org/10.1016/j.ymben.2014.09.008

    CAS  Article  PubMed  Google Scholar 

  109. Ledesma-Amaro R, Lazar Z, Rakicka M, Guo Z, Fouchard F, Coq A-MC-L, Nicaud J-M (2016) Metabolic engineering of Yarrowia lipolytica to produce chemicals and fuels from xylose. Metab Eng 38:115–124. https://doi.org/10.1016/j.ymben.2016.07.001

    CAS  Article  PubMed  Google Scholar 

  110. Lee H (1998) The structure and function of yeast xylose (aldose) reductases. Yeast 14(11):977–984. https://doi.org/10.1002/(sici)1097-0061(199808)14:11<977::aid-yea302>3.0.co;2-j

    CAS  Article  PubMed  Google Scholar 

  111. Lee J-K, Koo B-S, Kim S-Y (2002) Fumarate-mediated inhibition of erythrose reductase, a key enzyme for erythritol production by Torula corallina. Appl Environ Microbiol 68(9):4534–4538

    CAS  Article  Google Scholar 

  112. Lee J-K, Kim S-Y, Ryu Y-W, Seo J-H, Kim J-H (2003a) Purification and characterization of a novel erythrose reductase from Candida magnoliae. Appl Environ Microbiol 69(7):3710–3718

    CAS  Article  Google Scholar 

  113. Lee J-K, Koo B-S, Kim S-Y (2003b) Cloning and characterization of the xyl1 gene, encoding an NADH-preferring xylose reductase from Candida parapsilosis, and its functional expression in Candida tropicalis. Appl Environ Microbiol 69(10):6179–6188

    CAS  Article  Google Scholar 

  114. Lee JY, Kang CD, Lee SH, Park YK, Cho KM (2015) Engineering cellular redox balance in Saccharomyes cerevisiae for improved production of L-lactic acid. Biotechnol Bioeng 112(4):751–758. https://doi.org/10.1002/bit.25488

    CAS  Article  PubMed  Google Scholar 

  115. Li H, Alper HS (2016) Enabling xylose utilization in Yarrowia lipolytica for lipid production. Biotechnol J 11(9):1230–1240. https://doi.org/10.1002/biot.201600210

    CAS  Article  PubMed  Google Scholar 

  116. Li Q, Du W, Liu D (2008) Perspectives of microbial oils for biodiesel production. Appl Microbiol Biotechnol 80(5):749–756

    CAS  Article  Google Scholar 

  117. Lian J, Zhao H (2015) Recent advances in biosynthesis of fatty acids derived products in Saccharomyes cerevisiae via enhanced supply of precursor metabolites. J Ind Microbiol Biotechnol 42(3):437–451. https://doi.org/10.1007/s10295-014-1518-0

    CAS  Article  PubMed  Google Scholar 

  118. Lin Y, Tanaka S (2006) Ethanol fermentation from biomass resources: current state and prospects. Appl Microbiol Biotechnol 69(6):627–642. https://doi.org/10.1007/s00253-005-0229-x

    CAS  Article  PubMed  Google Scholar 

  119. Lin C-C, Hsieh P-C, Mau J-L, Teng D-F (2005) Construction of an intergeneric fusion from Schizosaccharomyces pombe and Lentinula edodes for xylan degradation and polyol production. Enzym Microb Technol 36(1):107–117. https://doi.org/10.1016/j.enzmictec.2004.07.007

    CAS  Article  Google Scholar 

  120. Lin J, Li S, Sun M, Zhang C, Yang W, Zhang Z, Li X, Li S (2014) Microbial lipid production by oleaginous yeast in d-xylose solution using a two-stage culture mode. RSC Adv 4(66):34944–34949. https://doi.org/10.1039/C4RA01453G

    CAS  Article  Google Scholar 

  121. Liu HH, Ji XJ, Huang H (2015) Biotechnological applications of Yarrowia lipolytica: past, present and future. Biotechnol Adv 33(8):1522–1546. https://doi.org/10.1016/j.biotechadv.2015.07.010

    CAS  Article  PubMed  Google Scholar 

  122. Liu Y, Koh CMJ, Yap SA, Du M, Hlaing MM, Ji L (2018) Identification of novel genes in the carotenogenic and oleaginous yeast Rhodotorula toruloides through genome-wide insertional mutagenesis. BMC Microbiol 18(1):14. https://doi.org/10.1186/s12866-018-1151-6

    Article  PubMed  PubMed Central  Google Scholar 

  123. Livesey G (2001) Tolerance of low-digestible carbohydrates: a general view. Br J Nutr 85(S1):S7–S16

    CAS  Article  Google Scholar 

  124. Maddox IS, Spencer K, Greenwood JM, Dawson MW, Brooks JD (1985) Production of citric acid from sugars present in wood hemicellulose using Aspergillus niger and Saccharomycopsis lipolytica. Biotechnol Lett 7(11):815–818. https://doi.org/10.1007/bf01025561

    CAS  Article  Google Scholar 

  125. Madhavan A, Tamalampudi S, Ushida K, Kanai D, Katahira S, Srivastava A, Fukuda H, Bisaria VS, Kondo A (2008) Xylose isomerase from polycentric fungus Orpinomyces: gene sequencing, cloning, and expression in Saccharomyes cerevisiae for bioconversion of xylose to ethanol. Appl Microbiol Biotechnol 82(6):1067–1078. https://doi.org/10.1007/s00253-008-1794-6

    CAS  Article  PubMed  Google Scholar 

  126. Mäkinen K, Saag M, Isotupa K, Olak J, Nõmmela R, Söderling E, Mäkinen P-L (2005) Similarity of the effects of erythritol and xylitol on some risk factors of dental caries. Caries Res 39(3):207–215

    Article  Google Scholar 

  127. Mamatha S, Ravi R, Venkateswaran G (2008) Medium optimization of gamma linolenic acid production in Mucor rouxii CFR-G15 using RSM. Food Bioprocess Technol 1(4):405–409

    Article  Google Scholar 

  128. Matsushika A, Inoue H, Kodaki T, Sawayama S (2009) Ethanol production from xylose in engineered Saccharomyes cerevisiae strains: current state and perspectives. Appl Microbiol Biotechnol 84(1):37–53. https://doi.org/10.1007/s00253-009-2101-x

    CAS  Article  PubMed  Google Scholar 

  129. Matthaus F, Ketelhot M, Gatter M, Barth G (2014) Production of lycopene in the non-carotenoid-producing yeast Yarrowia lipolytica. Appl Environ Microbiol 80(5):1660–1669. https://doi.org/10.1128/aem.03167-13

    Article  PubMed  PubMed Central  Google Scholar 

  130. Meijer MM, Boonstra J, Verkleij AJ, Verrips CT (1998) Glucose repression in Saccharomyes cerevisiae is related to the glucose concentration rather than the glucose flux. J Biol Chem 273(37):24102–24107

    CAS  Article  Google Scholar 

  131. Millati R, Edebo L, Taherzadeh MJ (2005) Performance of Rhizopus, Rhizomucor, and Mucor in ethanol production from glucose, xylose, and wood hydrolyzates. Enzym Microb Technol 36(2):294–300. https://doi.org/10.1016/j.enzmictec.2004.09.007

    CAS  Article  Google Scholar 

  132. Mirończuk AM, Biegalska A, Dobrowolski A (2017) Functional overexpression of genes involved in erythritol synthesis in the yeast Yarrowia lipolytica. Biotechnol Biofuels 10(1):77

    Article  Google Scholar 

  133. Misawa N, Shimada H (1997) Metabolic engineering for the production of carotenoids in non-carotenogenic bacteria and yeasts. J Biotechnol 59(3):169–181

    CAS  Article  Google Scholar 

  134. Mohd Azhar SH, Abdulla R, Jambo SA, Marbawi H, Gansau JA, Mohd Faik AA, Rodrigues KF (2017) Yeasts in sustainable bioethanol production: a review. Biochem Biophys Rep 10(Supplement C):52–61. https://doi.org/10.1016/j.bbrep.2017.03.003

    Article  PubMed  PubMed Central  Google Scholar 

  135. Moliné M, Libkind D, van Broock M (2012) Production of torularhodin, torulene, and β-carotene by Rhodotorula yeasts. In: Barredo J-L (ed) Microbial carotenoids from fungi: methods and protocols. Humana, Totowa, pp 275–283

    Chapter  Google Scholar 

  136. Moon H-J, Jeya M, Kim I-W, Lee J-K (2010) Biotechnological production of erythritol and its applications. Appl Microbiol Biotechnol 86(4):1017–1025. https://doi.org/10.1007/s00253-010-2496-4

    CAS  Article  PubMed  Google Scholar 

  137. Moran JW, Witter LD (1979) Effect of sugars on D-arabitol production and glucose metabolism in Saccharomyces rouxii. J Bacteriol 138(3):823–831

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Moysés DN, Reis VCB, de Almeida JRM, de Moraes LMP, Torres FAG (2016) Xylose fermentation by Saccharomyes cerevisiae: challenges and prospects. Int J Mol Sci 17(3):207. https://doi.org/10.3390/ijms17030207

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  139. Nabors L, Gelardi R (2001) Alternative sweeteners: an overview, 2nd edn. Marcel Dekker, New York, pp 1–10

    Google Scholar 

  140. Nevoigt E (2008) Progress in metabolic engineering of Saccharomyes cerevisiae. Microbiol Mol Biol Rev 72(3):379–412. https://doi.org/10.1128/MMBR.00025-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  141. Niehus X, Crutz-Le Coq A-M, Sandoval G, Nicaud J-M, Ledesma-Amaro R (2018) Engineering Yarrowia lipolytica to enhance lipid production from lignocellulosic materials. Biotechnol Biofuels 11(1):11. https://doi.org/10.1186/s13068-018-1010-6

    Article  PubMed  PubMed Central  Google Scholar 

  142. Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen J, Heidelberg JF, Alley MRK, Ohta N, Maddock JR, Potocka I, Nelson WC, Newton A, Stephens C, Phadke ND, Ely B, DeBoy RT, Dodson RJ, Durkin AS, Gwinn ML, Haft DH, Kolonay JF, Smit J, Craven MB, Khouri H, Shetty J, Berry K, Utterback T, Tran K, Wolf A, Vamathevan J, Ermolaeva M, White O, Salzberg SL, Venter JC, Shapiro L, Fraser CM (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A 98(7):4136–4141. https://doi.org/10.1073/pnas.061029298

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  143. Nunn CE, Johnsen U, Schonheit P, Fuhrer T, Sauer U, Hough DW, Danson MJ (2010) Metabolism of pentose sugars in the hyperthermophilic archaea Sulfolobus solfataricus and Sulfolobus acidocaldarius. J Biol Chem 285(44):33701–33709. https://doi.org/10.1074/jbc.M110.146332

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  144. Nyyssölä A, Pihlajaniemi A, Palva A, Von Weymarn N, Leisola M (2005) Production of xylitol from D-xylose by recombinant Lactococcus lactis. J Biotechnol 118(1):55–66

    Article  Google Scholar 

  145. Oh D-K, Kim S-Y (1998) Increase of xylitol yield by feeding xylose and glucose in Candida tropicalis. Appl Microbiol Biotechnol 50(4):419–425. https://doi.org/10.1007/s002530051314

    CAS  Article  PubMed  Google Scholar 

  146. Oh EJ, Ha SJ, Rin Kim S, Lee WH, Galazka JM, Cate JH, Jin YS (2013) Enhanced xylitol production through simultaneous co-utilization of cellobiose and xylose by engineered Saccharomyes cerevisiae. Metab Eng 15:226–234. https://doi.org/10.1016/j.ymben.2012.09.003

    CAS  Article  PubMed  Google Scholar 

  147. Pal S, Mondal AK, Sahoo DK (2016) Molecular strategies for enhancing microbial production of xylitol. Process Biochem 51(7):809–819. https://doi.org/10.1016/j.procbio.2016.03.017

    CAS  Article  Google Scholar 

  148. Papagianni M (2012) Metabolic engineering of lactic acid bacteria for the production of industrially important compounds. Comput Struct Biotechnol J 3:e201210003. https://doi.org/10.5936/csbj.201210003

    Article  PubMed  PubMed Central  Google Scholar 

  149. Papanikolaou S, Aggelis G (2011) Lipids of oleaginous yeasts. Part I: biochemistry of single cell oil production. Eur J Lipid Sci Technol 113(8):1031–1051

    CAS  Article  Google Scholar 

  150. Parajo JC, Santos V, Vazquez M (1997) Co-production of carotenoids and xylitol by Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Biotechnol Lett 19(2):139–142. https://doi.org/10.1023/a:1018356113002

    CAS  Article  Google Scholar 

  151. Parajó JC, Santos V, Vázquez M (1998) Optimization of carotenoid production by Phaffia rhodozyma cells grown on xylose. Process Biochem 33(2):181–187. https://doi.org/10.1016/S0032-9592(97)00045-9

    Article  Google Scholar 

  152. Park YK, Nicaud JM, Ledesma-Amaro R (2017) The engineering potential of Rhodosporidium toruloides as a workhorse for biotechnological applications. Trends Biotechnol 36:304–317. https://doi.org/10.1016/j.tibtech.2017.10.013

    CAS  Article  PubMed  Google Scholar 

  153. Porro D, Brambilla L, Ranzi BM, Martegani E, Alberghina L (1995) Development of metabolically engineered Saccharomyes cerevisiae cells for the production of lactic acid. Biotechnol Prog 11(3):294–298. https://doi.org/10.1021/bp00033a009

    CAS  Article  PubMed  Google Scholar 

  154. Rafiqul ISM, Sakinah AMM (2012) Design of process parameters for the production of xylose from wood sawdust. Chem Eng Res Des 90(9):1307–1312. https://doi.org/10.1016/j.cherd.2011.12.009

    CAS  Article  Google Scholar 

  155. Rafiqul ISM, Sakinah AMM (2013) Processes for the production of xylitol—a review. Food Rev Int 29(2):127–156. https://doi.org/10.1080/87559129.2012.714434

    CAS  Article  Google Scholar 

  156. Rangaswamy S, Agblevor F (2002) Screening of facultative anaerobic bacteria utilizing D-xylose for xylitol production. Appl Microbiol Biotechnol 60(1–2):88–93

    CAS  PubMed  Google Scholar 

  157. Rao RS, Bhadra B, Shivaji S (2007) Isolation and characterization of xylitol-producing yeasts from the gut of colleopteran insects. Curr Microbiol 55(5):441–446. https://doi.org/10.1007/s00284-007-9005-8

    CAS  Article  PubMed  Google Scholar 

  158. Ratledge C (2004) Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86(11):807–815. https://doi.org/10.1016/j.biochi.2004.09.017

    CAS  Article  PubMed  Google Scholar 

  159. Ribeiro O, Domingues L, Penttilä M, Wiebe MG (2012) Nutritional requirements and strain heterogeneity in Ashbya gossypii. J Basic Microbiol 52(5):582–589. https://doi.org/10.1002/jobm.201100383

    CAS  Article  PubMed  Google Scholar 

  160. Rodriguez GM, Hussain MS, Gambill L, Gao D, Yaguchi A, Blenner M (2016) Engineering xylose utilization in Yarrowia lipolytica by understanding its cryptic xylose pathway. Biotechnol Biofuels 9(1):149. https://doi.org/10.1186/s13068-016-0562-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  161. Ruan Z, Zanotti M, Wang X, Ducey C, Liu Y (2012) Evaluation of lipid accumulation from lignocellulosic sugars by Mortierella isabellina for biodiesel production. Bioresour Technol 110:198–205

    CAS  Article  Google Scholar 

  162. Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454:841–845. https://doi.org/10.1038/nature07190

    CAS  Article  PubMed  Google Scholar 

  163. Rupilius W, Ahmad S (2007) Palm oil and palm kernel oil as raw materials for basic oleochemicals and biodiesel. Eur J Lipid Sci Technol 109(4):433–439. https://doi.org/10.1002/ejlt.200600291

    CAS  Article  Google Scholar 

  164. Ryu S, Hipp J, Trinh CT (2015) Activating and elucidating metabolism of complex sugars in Yarrowia lipolytica. Appl Environ Microbiol 82(4):1334–1345. https://doi.org/10.1128/aem.03582-15

    Article  PubMed  Google Scholar 

  165. Rywińska A, Rymowicz W, Żarowska B, Skrzypiński A (2010) Comparison of citric acid production from glycerol and glucose by different strains of Yarrowia lipolytica. World J Microbiol Biotechnol 26(7):1217–1224. https://doi.org/10.1007/s11274-009-0291-0

    CAS  Article  PubMed  Google Scholar 

  166. Rzechonek DA, Dobrowolski A, Rymowicz W, Mirończuk AM (2018) Recent advances in biological production of erythritol. Crit Rev Biotechnol 38(4):620–633. https://doi.org/10.1080/07388551.2017.1380598

    CAS  Article  PubMed  Google Scholar 

  167. Saha BC, Bothast RJ (1997) Microbial production of xylitol fuels and chemicals from biomass. ACS Symposium Series, vol 666. American Chemical Society, pp 307–319

  168. Saha BC, Sakakibara Y, Cotta MA (2007) Production of d-arabitol by a newly isolated Zygosaccharomyces rouxii. J Ind Microbiol Biotechnol 34(7):519–523. https://doi.org/10.1007/s10295-007-0211-y

    CAS  Article  PubMed  Google Scholar 

  169. Saloheimo A, Rauta J, Stasyk OV, Sibirny AA, Penttila M, Ruohonen L (2007) Xylose transport studies with xylose-utilizing Saccharomyes cerevisiae strains expressing heterologous and homologous permeases. Appl Microbiol Biotechnol 74(5):1041–1052. https://doi.org/10.1007/s00253-006-0747-1

    CAS  Article  PubMed  Google Scholar 

  170. Salusjärvi L, Kankainen M, Soliymani R, Pitkänen J-P, Penttilä M, Ruohonen L (2008) Regulation of xylose metabolism in recombinant Saccharomyes cerevisiae. Microb Cell Factories 7(1):18. https://doi.org/10.1186/1475-2859-7-18

    CAS  Article  Google Scholar 

  171. Sampaio FC, Silveira WB, Chaves-Alves VM, Passos FML, Coelho JLC (2003) Screening of filamentous fungi for production of xylitol from D-xylose. Braz J Microbiol 34:321–324

    Article  Google Scholar 

  172. Sampaio FC, Chaves-Alves VM, Converti A, Lopes Passos FM, Cavalcante Coelho JL (2008) Influence of cultivation conditions on xylose-to-xylitol bioconversion by a new isolate of Debaryomyces hansenii. Bioresour Technol 99(3):502–508. https://doi.org/10.1016/j.biortech.2007.01.017

    CAS  Article  PubMed  Google Scholar 

  173. Sarthy AV, McConaughy BL, Lobo Z, Sundstrom JA, Furlong CE, Hall BD (1987) Expression of the Escherichia coli xylose isomerase gene in Saccharomyes cerevisiae. Appl Environ Microbiol 53(9):1996–2000

    CAS  PubMed  PubMed Central  Google Scholar 

  174. Sasaki M, Jojima T, Inui M, Yukawa H (2010) Xylitol production by recombinant Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biotechnol 86(4):1057–1066

    CAS  Article  Google Scholar 

  175. Schellenberg GD, Sarthy A, Larson AE, Backer MP, Crabb JW, Lidstrom M, Hall BD, Furlong CE (1984) Xylose isomerase from Escherichia coli. Characterization of the protein and the structural gene. J Biol Chem 259(11):6826–6832

    CAS  PubMed  Google Scholar 

  176. Schneider H, Lee H, Barbosa Mde F, Kubicek CP, James AP (1989) Physiological properties of a mutant of Pachysolen tannophilus deficient in NADPH-dependent d-xylose reductase. Appl Environ Microbiol 55(11):2877–2881

    CAS  PubMed  PubMed Central  Google Scholar 

  177. Seip J, Jackson R, He H, Zhu Q, Hong SP (2013) Snf1 is a regulator of lipid accumulation in Yarrowia lipolytica. Appl Environ Microbiol 79(23):7360–7370. https://doi.org/10.1128/aem.02079-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  178. Shi S, Zhao H (2017) Metabolic engineering of oleaginous yeasts for production of fuels and chemicals. Front Microbiol 8:2185. https://doi.org/10.3389/fmicb.2017.02185

    Article  PubMed  PubMed Central  Google Scholar 

  179. Shi S, Chen Y, Siewers V, Nielsen J (2014) Improving production of malonyl coenzyme A-derived metabolites by abolishing Snf1-dependent regulation of Acc1. MBio 5(3):e01130–e01114. https://doi.org/10.1128/mBio.01130-14

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  180. Shiba Y, Paradise EM, Kirby J, Ro D-K, Keasling JD (2007) Engineering of the pyruvate dehydrogenase bypass in Saccharomyes cerevisiae for high-level production of isoprenoids. Metab Eng 9(2):160–168. https://doi.org/10.1016/j.ymben.2006.10.005

    CAS  Article  PubMed  Google Scholar 

  181. Skory CD (2003) Lactic acid production by Saccharomyes cerevisiae expressing a Rhizopus oryzae lactate dehydrogenase gene. J Ind Microbiol Biotechnol 30(1):22–27. https://doi.org/10.1007/s10295-002-0004-2

    CAS  Article  PubMed  Google Scholar 

  182. Spencer J, Sallans H (1956) Production of polyhydric alcohols by osmophilic yeasts. Can J Microbiol 2(2):72–79

    CAS  Article  Google Scholar 

  183. Stephen Dahms A (1974) 3-Deoxy-D-pentulosonic acid aldolase and its role in a new pathway of D-xylose degradation. Biochem Biophys Res Commun 60(4):1433–1439. https://doi.org/10.1016/0006-291X(74)90358-1

    Article  Google Scholar 

  184. Stephens C, Christen B, Fuchs T, Sundaram V, Watanabe K, Jenal U (2007) Genetic analysis of a novel pathway for D-xylose metabolism in Caulobacter crescentus. J Bacteriol 189(5):2181–2185. https://doi.org/10.1128/jb.01438-06

    CAS  Article  PubMed  Google Scholar 

  185. Stincone A, Prigione A, Cramer T, Wamelink MMC, Campbell K, Cheung E, Olin-Sandoval V, Grüning N-M, Krüger A, Tauqeer Alam M, Keller MA, Breitenbach M, Brindle KM, Rabinowitz JD, Ralser M (2015) The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev 90(3):927–963. https://doi.org/10.1111/brv.12140

    Article  PubMed  Google Scholar 

  186. Suryadi H, Katsuragi T, Yoshida N, Suzuki S, Tani Y (2000) Polyol production by culture of methanol-utilizing yeast. J Biosci Bioeng 89(3):236–240

    CAS  Article  Google Scholar 

  187. Suzuki T, S-i Y, Kinoshita Y, Yamada H, Hatsu M, Takamizawa K, Kawai K (1999) Expression of xyrA gene encoding for D-xylose reductase of Candida tropicalis and production of xylitol in Escherichia coli. J Biosci Bioeng 87(3):280–284

    CAS  Article  Google Scholar 

  188. Tai Y-S, Xiong M, Jambunathan P, Wang J, Wang J, Stapleton C, Zhang K (2016) Engineering nonphosphorylative metabolism to generate lignocellulose-derived products. Nat Chem Biol 12:247–253. https://doi.org/10.1038/nchembio.2020 https://www.nature.com/articles/nchembio.2020#supplementary-information

    CAS  Article  PubMed  Google Scholar 

  189. Tippmann S, Chen Y, Siewers V, Nielsen J (2013) From flavors and pharmaceuticals to advanced biofuels: production of isoprenoids in Saccharomyes cerevisiae. Biotechnol J 8(12):1435–1444. https://doi.org/10.1002/biot.201300028

    CAS  Article  PubMed  Google Scholar 

  190. Toivari MH, Salusjärvi L, Ruohonen L, Penttilä M (2004) Endogenous xylose pathway in Saccharomyes cerevisiae. Appl Environ Microbiol 70(6):3681–3686. https://doi.org/10.1128/AEM.70.6.3681-3686.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  191. Toivola A, Yarrow D, van den Bosch E, van Dijken JP, Scheffers WA (1984) Alcoholic fermentation of d-xylose by yeasts. Appl Environ Microbiol 47(6):1221–1223

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Turner TL, Zhang GC, Kim SR, Subramaniam V, Steffen D, Skory CD, Jang JY, Yu BJ, Jin YS (2015) Lactic acid production from xylose by engineered Saccharomyes cerevisiae without PDC or ADH deletion. Appl Microbiol Biotechnol 99(19):8023–8033. https://doi.org/10.1007/s00253-015-6701-3

    CAS  Article  PubMed  Google Scholar 

  193. Turner TL, Kim E, Hwang C, Zhang G-C, Liu J-J, Jin Y-S (2017) Conversion of lactose and whey into lactic acid by engineered yeast. J Dairy Sci 100(1):124–128. https://doi.org/10.3168/jds.2016-11784

    CAS  Article  PubMed  Google Scholar 

  194. Umemoto Y, Shibata T, Araki T (2012) D-xylose isomerase from a marine bacterium, Vibrio sp. strain XY-214, and D-xylulose production from β-1,3-xylan. Mar Biotechnol 14(1):10–20. https://doi.org/10.1007/s10126-011-9380-9

    CAS  Article  PubMed  Google Scholar 

  195. Upton DJ, McQueen-Mason SJ, Wood AJ (2017) An accurate description of Aspergillus niger organic acid batch fermentation through dynamic metabolic modelling. Biotechnol Biofuels 10:258. https://doi.org/10.1186/s13068-017-0950-6

    Article  PubMed  PubMed Central  Google Scholar 

  196. Van Eck JH, Prior BA, Brandt EV (1993) The water relations of growth and polyhydroxy alcohol production by ascomycetous yeasts. Microbiol 139(5):1047–1054. https://doi.org/10.1099/00221287-139-5-1047

    Article  Google Scholar 

  197. van Zyl C, Prior BA, Kilian SG, Kock JL (1989) D-xylose utilization by Saccharomyes cerevisiae. J Gen Microbiol 135(11):2791–2798. https://doi.org/10.1099/00221287-135-11-2791

    Article  PubMed  Google Scholar 

  198. Vandeska E, Amartey S, Kuzmanova S, Jeffries T (1995) Effects of environmental conditions on production of xylitol by Candida boidinii. World J Microbiol Biotechnol 11(2):213–218. https://doi.org/10.1007/bf00704652

    CAS  Article  PubMed  Google Scholar 

  199. Veiga-da-Cunha M, Santos H, Van Schaftingen E (1993) Pathway and regulation of erythritol formation in Leuconostoc oenos. J Bacteriol 175(13):3941–3948

    CAS  Article  Google Scholar 

  200. Walfridsson M, Bao X, Anderlund M, Lilius G, Bulow L, Hahn-Hagerdal B (1996) Ethanolic fermentation of xylose with Saccharomyes cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase. Appl Environ Microbiol 62(12):4648–4651

    CAS  PubMed  PubMed Central  Google Scholar 

  201. Walfridsson M, Anderlund M, Bao X, Hahn-Hägerdal B (1997) Expression of different levels of enzymes from the Pichia stipitis XYL1 and XYL2 genes in Saccharomyes cerevisiae and its effects on product formation during xylose utilisation. Appl Microbiol Biotechnol 48(2):218–224

    CAS  Article  Google Scholar 

  202. Waltermann M, Steinbuchel A (2005) Neutral lipid bodies in prokaryotes: recent insights into structure, formation, and relationship to eukaryotic lipid depots. J Bacteriol 187(11):3607–3619. https://doi.org/10.1128/jb.187.11.3607-3619.2005

    Article  PubMed  PubMed Central  Google Scholar 

  203. Wang TH, Zhong YH, Huang W, Liu T, You YW (2005) Antisense inhibition of xylitol dehydrogenase gene, xdh1 from Trichoderma reesei. Lett Appl Microbiol 40(6):424–429. https://doi.org/10.1111/j.1472-765X.2005.01685.x

    CAS  Article  PubMed  Google Scholar 

  204. Wang Y, Zhang S, Zhu Z, Shen H, Lin X, Jin X, Jiao X, Zhao ZK (2018) Systems analysis of phosphate-limitation-induced lipid accumulation by the oleaginous yeast Rhodosporidium toruloides. Biotechnol Biofuels 11(1):148. https://doi.org/10.1186/s13068-018-1134-8

    Article  PubMed  PubMed Central  Google Scholar 

  205. Weete JD (2012) Lipid biochemistry of fungi and other organisms. Media Plenum, New York

    Google Scholar 

  206. Weimberg R (1961) Pentose oxidation by Pseudomonas fragi. J Biol Chem 236:629–635

    CAS  PubMed  Google Scholar 

  207. Werpy T, Petersen G, Aden A, Bozell J, Holladay J, White J, Manheim A, Eliot D, Lasure L, Jones S (2004) Top value added chemicals from biomass. Volume 1—results of screening for potential candidates from sugars and synthesis gas. Department of Energy Washington DC

  208. Weyda I, Lubeck M, Ahring BK, Lubeck PS (2014) Point mutation of the xylose reductase (XR) gene reduces xylitol accumulation and increases citric acid production in Aspergillus carbonarius. J Ind Microbiol Biotechnol 41(4):733–739. https://doi.org/10.1007/s10295-014-1415-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  209. Whitworth DA, Ratledge C (1977) Phosphoketolase in Rhodotorula graminis and other yeasts. Microbiology 102(2):397–401. https://doi.org/10.1099/00221287-102-2-397

    CAS  Article  Google Scholar 

  210. Wilson BL, Mortlock RP (1973) Regulation of D-xylose and D-arabitol catabolism by Aerobacter aerogenes. J Bacteriol 113(3):1404–1411

    CAS  PubMed  PubMed Central  Google Scholar 

  211. Xiong X, Wang X, Chen S (2012) Engineering of a xylose metabolic pathway in Rhodococcus strains. Appl Environ Microbiol 78(16):5483–5491. https://doi.org/10.1128/AEM.08022-11

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  212. Xu H, Kim S, Sorek H, Lee Y, Jeong D, Kim J, Oh EJ, Yun EJ, Wemmer DE, Kim KH, Kim SR, Jin Y-S (2016) PHO13 deletion-induced transcriptional activation prevents sedoheptulose accumulation during xylose metabolism in engineered Saccharomyes cerevisiae. Metab Eng 34:88–96. https://doi.org/10.1016/j.ymben.2015.12.007

    CAS  Article  PubMed  Google Scholar 

  213. Xue Z, Sharpe PL, Hong SP, Yadav NS, Xie D, Short DR, Damude HG, Rupert RA, Seip JE, Wang J, Pollak DW, Bostick MW, Bosak MD, Macool DJ, Hollerbach DH, Zhang H, Arcilla DM, Bledsoe SA, Croker K, McCord EF, Tyreus BD, Jackson EN, Zhu Q (2013) Production of omega-3 eicosapentaenoic acid by metabolic engineering of Yarrowia lipolytica. Nat Biotechnol 31(8):734–740. https://doi.org/10.1038/nbt.2622

    CAS  Article  PubMed  Google Scholar 

  214. Yaguchi A, Spagnuolo M, Blenner M (2018) Engineering yeast for utilization of alternative feedstocks. Curr Opin Biotechnol 53:122–129. https://doi.org/10.1016/j.copbio.2017.12.003

    CAS  Article  PubMed  Google Scholar 

  215. Yamada R, Yamauchi A, Kashihara T, Ogino H (2017) Evaluation of lipid production from xylose and glucose/xylose mixed sugar in various oleaginous yeasts and improvement of lipid production by UV mutagenesis. Biochem Eng J 128:76–82. https://doi.org/10.1016/j.bej.2017.09.010

    CAS  Article  Google Scholar 

  216. Yang X, Lai Z, Lai C, Zhu M, Li S, Wang J, Wang X (2013) Efficient production of l-lactic acid by an engineered Thermoanaerobacterium aotearoense with broad substrate specificity. Biotechnol Biofuels 6(1):124. https://doi.org/10.1186/1754-6834-6-124

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  217. Yoshitake J, Ishizaki H, Shimamura M, Imai T (1973) Xylitol production by an Enterobacter species. Agric Biol Chem 37(10):2261–2267

    CAS  Article  Google Scholar 

  218. Zaldivar J, Nielsen J, Olsson L (2001) Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56(1):17–34. https://doi.org/10.1007/s002530100624

    CAS  Article  PubMed  Google Scholar 

  219. Zha J, Li B-Z, Shen M-H, Hu M-L, Song H, Yuan Y-J (2013) Optimization of CDT-1 and XYL1 expression for balanced co-production of ethanol and xylitol from cellobiose and xylose by engineered Saccharomyes cerevisiae. PLoS One 8(7):e68317

    CAS  Article  Google Scholar 

  220. Zhang M, Eddy C, Deanda K, Finkelstein M, Picataggio S (1995) Metabolic engineering of a pentose metabolism pathway in ethanologenic Zymomonas mobilis. Science 267(5195):240–243. https://doi.org/10.1126/science.267.5195.240

    CAS  Article  PubMed  Google Scholar 

  221. Zhang Z, Yeung WK, Huang Y, Chen ZY (2002) Effect of squalene and shark liver oil on serum cholesterol level in hamsters. Int J Food Sci Nutr 53(5):411–418. https://doi.org/10.1080/0963748021000044750

    CAS  Article  PubMed  Google Scholar 

  222. Zhang B, Li L, Zhang J, Gao X, Wang D, Hong J (2013) Improving ethanol and xylitol fermentation at elevated temperature through substitution of xylose reductase in Kluyveromyces marxianus. J Ind Microbiol Biotechnol 40(3–4):305–316

    CAS  Article  Google Scholar 

  223. Zhang J, Zhang B, Wang D, Gao X, Hong J (2014) Xylitol production at high temperature by engineered Kluyveromyces marxianus. Bioresour Technol 152:192–201

    CAS  Article  Google Scholar 

  224. Zhang J, Zhang B, Wang D, Gao X, Hong J (2015) Improving xylitol production at elevated temperature with engineered Kluyveromyces marxianus through over-expressing transporters. Bioresour Technol 175:642–645

    CAS  Article  Google Scholar 

  225. Zhang S, Ito M, Skerker JM, Arkin AP, Rao CV (2016a) Metabolic engineering of the oleaginous yeast Rhodosporidium toruloides IFO0880 for lipid overproduction during high-density fermentation. Appl Microbiol Biotechnol 100(21):9393–9405. https://doi.org/10.1007/s00253-016-7815-y

    CAS  Article  PubMed  Google Scholar 

  226. Zhang S, Skerker JM, Rutter CD, Maurer MJ, Arkin AP, Rao CV (2016b) Engineering Rhodosporidium toruloides for increased lipid production. Biotechnol Bioeng 113(5):1056–1066. https://doi.org/10.1002/bit.25864

    CAS  Article  PubMed  Google Scholar 

  227. Zheng Y, Yu X, Zeng J, Chen S (2012) Feasibility of filamentous fungi for biofuel production using hydrolysate from dilute sulfuric acid pretreatment of wheat straw. Biotechnol Biofuels 5(1):50. https://doi.org/10.1186/1754-6834-5-50

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  228. Zhou J, Wu K, Rao CV (2016) Evolutionary engineering of Geobacillus thermoglucosidasius for improved ethanol production. Biotechnol Bioeng 113(10):2156–2167. https://doi.org/10.1002/bit.25983

    CAS  Article  PubMed  Google Scholar 

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This material is based upon the work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number(s) DE-SC0018420.

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Jagtap, S.S., Rao, C.V. Microbial conversion of xylose into useful bioproducts. Appl Microbiol Biotechnol 102, 9015–9036 (2018). https://doi.org/10.1007/s00253-018-9294-9

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Keywords

  • Hemicellulose
  • Xylose
  • Fermentation
  • Metabolic engineering
  • Bioproducts