Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Metabolic Engineering for Improved Fermentation of L-Arabinose

  • Ye, Suji (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Kim, Jeong-won (School of Food Science and Biotechnology, Kyungpook National University) ;
  • Kim, Soo Rin (School of Food Science and Biotechnology, Kyungpook National University)
  • Received : 2018.12.10
  • Accepted : 2019.01.29
  • Published : 2019.03.28
Download PDF
⟨ Previous Next ⟩

Abstract

L-Arabinose, a five carbon sugar, has not been considered as an important bioresource because most studies have focused on D-xylose, another type of five-carbon sugar that is prevalent as a monomeric structure of hemicellulose. In fact, L-arabinose is also an important monomer of hemicellulose, but its content is much more significant in pectin (3-22%, g/g pectin), which is considered an alternative biomass due to its low lignin content and mass production as juice-processing waste. This review presents native and engineered microorganisms that can ferment L-arabinose. Saccharomyces cerevisiae is highlighted as the most preferred engineering host for expressing a heterologous arabinose pathway for producing ethanol. Because metabolic engineering efforts have been limited so far, with this review as momentum, more attention to research is needed on the fermentation of L-arabinose as well as the utilization of pectin-rich biomass.

Keywords

References

  1. Robertson GP, Hamilton SK, Barham BL, Dale BE, Izaurralde RC, Jackson RD, et al. 2017. Cellulosic biofuel contributions to a sustainable energy future: choices and outcomes. Science 356(6345).
  2. Girio FM, Fonseca C, Carvalheiro F, Duarte LC, Marques S, Bogel-Łukasik R. 2010. Hemicelluloses for fuel ethanol: a review. Bioresour. Technol. 101: 4775-4800. https://doi.org/10.1016/j.biortech.2010.01.088
  3. Go AR, Ko JW, Lee SJ, Kim SW, Han SO, Lee J, et al. 2012. Process design and evaluation of value-added chemicals production from biomass. Biotechnol. Bioprocess Eng. 17: 1055-1061. https://doi.org/10.1007/s12257-012-0257-1
  4. Trinh LTP, Lee Y-J, Lee J-W, Lee W-H. 2018. Optimization of ionic liquid pretreatment of mixed softwood by response surface methodology and reutilization of ionic liquid from hydrolysate. Biotechnol. Bioprocess Eng. 23: 228-237. https://doi.org/10.1007/s12257-017-0209-x
  5. Alonso DM, Hakim SH, Zhou S, Won W, Hosseinaei O, Tao J, et al. 2017. Increasing the revenue from lignocellulosic biomass: maximizing feedstock utilization. Science Adv. 3: e1603301. https://doi.org/10.1126/sciadv.1603301
  6. Liao JC, Mi L, Pontrelli S, Luo S. 2016. Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat. Rev. Microbiol. 14: 288-288. https://doi.org/10.1038/nrmicro.2016.32
  7. Wei N, Quarterman J, Jin YS. 2013. Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol. 31: 70-77. https://doi.org/10.1016/j.tibtech.2012.10.009
  8. Park M-R, Kim S-K, Jeong G-T. 2018. Biosugar production from Gracilaria verrucosa with sulfamic acid pretreatment and subsequent enzymatic hydrolysis. Biotechnol. Bioprocess Eng. 23: 302-310. https://doi.org/10.1007/s12257-018-0090-2
  9. Javier AG, Maria C ristina R, Oriana S, Maria E lena L. 2018. Saccharification of brown macroalgae using an arsenal of recombinant alginate lyases: potential application in the biorefinery process. J. Microbiol. Biotechnol. 28: 1671-1682. https://doi.org/10.4014/jmb.1805.05056
  10. Oh YR, Jung KA, Lee HJ, Jung GY, Park JM. 2018. A novel 3,6-anhydro-L-galactose dehydrogenase produced by a newly isolated Raoultella ornithinolytica B6-JMP12. Biotechnol. Bioprocess Eng. 23: 64-71. https://doi.org/10.1007/s12257-017-0480-x
  11. Van Dyk JS, Gama R, Morrison D, Swart S, Pletschke BI. 2013. Food processing waste: problems, current management and prospects for utilisation of the lignocellulose component through enzyme synergistic degradation. Renew. Sustain. Energy Rev. 26: 521-531. https://doi.org/10.1016/j.rser.2013.06.016
  12. Lisandro GS, Raul NC, Maria TB, Miguel AI. 2018. Feasibility of bioethanol production from cider waste. J. Microbiol. Biotechnol. 28: 1493-1501. https://doi.org/10.4014/jmb.1801.01044
  13. Edwards MC, Doran-Peterson J. 2012. Pectin-rich biomass as feedstock for fuel ethanol production. Appl. Microbiol. Biotechnol. 95: 565-575. https://doi.org/10.1007/s00253-012-4173-2
  14. Choi IS, Lee YG, Khanal SK, Park BJ, Bae HJ. 2015. A lowenergy, cost-effective approach to fruit and citrus peel waste processing for bioethanol production. App. Energy 140: 65-74. https://doi.org/10.1016/j.apenergy.2014.11.070
  15. May CD. 1990. Industrial pectins: Sources, production and applications. Carbohydr. Polym. 12: 79-99. https://doi.org/10.1016/0144-8617(90)90105-2
  16. Seiboth B, Metz B. 2011. Fungal arabinan and L-arabinose metabolism. Appl. Microbiol. Biotechnol. 89: 1665-1673. https://doi.org/10.1007/s00253-010-3071-8
  17. Oosterveld A, Beldman G, Schols HA, Voragen AGJ. 1996. Arabinose and ferulic acid rich pectic polysaccharides extracted from sugar beet pulp. Carbohydr. Res. 288: 143-153. https://doi.org/10.1016/0008-6215(96)00092-4
  18. Muller-Maatsch J, Bencivenni M, Caligiani A, Tedeschi T, Bruggeman G, Bosch M, et al. 2016. Pectin content and composition from different food waste streams in memory of Anna Surribas, scientist and friend. Food Chem. 201: 37-45. https://doi.org/10.1016/j.foodchem.2016.01.012
  19. van Maris AJA, Abbott DA, Bellissimi E, van den Brink J, Kuyper M, Luttik MAH, et al. 2006. Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie Van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 90: 391-418. https://doi.org/10.1007/s10482-006-9085-7
  20. Kim SR, Park YC, Jin YS, Seo JH. 2013. Strain engineering of Saccharomyces cerevisiae for enhanced xylose metabolism. Biotechnol. Adv. 31: 851-861. https://doi.org/10.1016/j.biotechadv.2013.03.004
  21. Hahn-Hagerdal B, Karhumaa K, Fonseca C, Spencer-Martins I, Gorwa-Grauslund MF. 2007. Towards industrial pentosefermenting yeast strains. Appl. Microbiol. Biotechnol. 74: 937-953. https://doi.org/10.1007/s00253-006-0827-2
  22. Servinsky MD, Germane KL, Liu S, Kiel JT, Clark AM, Shankar J, et al. 2012. Arabinose is metabolized via a phosphoketolase pathway in Clostridium acetobutylicum ATCC 824. J. Ind. Microbiol. Biotechnol. 39: 1859-1867. https://doi.org/10.1007/s10295-012-1186-x
  23. Fonseca C, Romao R, Rodrigues De Sousa H, Hahn-Hagerdal B, Spencer-Martins I. 2007. L-Arabinose transport and catabolism in yeast. FEBS J. 274: 3589-3600. https://doi.org/10.1111/j.1742-4658.2007.05892.x
  24. Verho R, Putkonen M, Londesborough J, Penttila M, Richard P. 2004. A novel NADH-linked L-xylulose reductase in the L-arabinose catabolic pathway of yeast. J. Biol. Chem. 279: 14746-14751. https://doi.org/10.1074/jbc.M312533200
  25. Fonseca C, Spencer-Martins I, Hahn-Hagerdal B. 2007. LArabinose metabolism in Candida arabinofermentans P YC C 5603T and Pichia guilliermondii PYCC 3012: influence of sugar and oxygen on product formation. Appl. Microbiol. Biotechnol. 75: 303-310. https://doi.org/10.1007/s00253-006-0830-7
  26. McMillan JD, Boynton BL. 1994. Arabinose utilization by xylose-fermenting yeasts and fungi. Appl. Biochem. Biotechnol. 45-46: 569-584. https://doi.org/10.1007/BF02941831
  27. Watanabe S, Kodak T, Makino K. 2006. Cloning, expression, and characterization of bacterial L-arabinose 1-dehydrogenase involved in an alternative pathway of L-arabinose metabolism. J. Biol. Chem. 281: 2612-2623 https://doi.org/10.1074/jbc.M506477200
  28. Dien BS, Kurtzman CP, Saha BC, Bothast RJ. 1996. Screening for L-arabinose fermenting yeasts. Appl. Biochem. Biotechnol. 57-58: 233-242. https://doi.org/10.1007/BF02941704
  29. Kurtzman CP, Dien BS. 1998. Candida arabinofermentans, a new L-arabinose fermenting yeast. Antonie Van Leeuwenhoek Int. J. Gen. Mol. Microbiol. 74: 237-243. https://doi.org/10.1023/A:1001799607871
  30. Wisselink HW, Toirkens MJ, Berriel MDRF, Winkler AA, Van Dijken JP, Pronk JT, et al. 2007. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of L-arabinose. Appl. Environ. Microbiol. 15: 488-491.
  31. Finn RK, Bringer S, Sahm H. 1984. Fermentation of arabinose to ethanol by Sarcina ventriculi. Appl. Microbiol. Biotechnol. 19: 161-166. https://doi.org/10.1007/BF00256448
  32. Bothast RJ, Saha BC, Flosenzier V, Ingram LO. 1994. Fermentation of L-arabinose, D-xylose and D-glucose by ethanologenic recombinant Klebsiella oxytoca strain P2. Biotechnol. Lett. 16: 401-406. https://doi.org/10.1007/BF00245060
  33. Dien BS, Hespell RB, Wyckoff HA, Bothast RJ. 1998. Fermentation of hexoses and pentoses sugars using a novel ethanologenic Escherichia coli strain. Enzyme Microb. Technol. 23: 366-371. https://doi.org/10.1016/S0141-0229(98)00064-7
  34. Richard P, Verho R, Putkonen M, Londesborough J, Penttila M. 2003. Production of ethanol from L-arabinose by Saccharomyces cerevisiae containing a fungal L-arabinose pathway. FEMS Yeast Res. 3: 185-189. https://doi.org/10.1016/S1567-1356(02)00184-8
  35. Bera AK, Sedlak M, Khan A, Ho NWY. 2010. Establishment of L-arabinose fermentation in glucose/xylose co-fermenting recombinant Saccharomyces cerevisiae 424A(LNH-ST) by genetic engineering. Appl. Microbiol. Biotechnol. 87: 1803-1811. https://doi.org/10.1007/s00253-010-2609-0
  36. Becker J, Boles E. 2003. A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Appl. Environ. Microbiol. 69: 4144-4150. https://doi.org/10.1128/AEM.69.7.4144-4150.2003
  37. Wang C, Shen Y, Zhang Y, Suo F, Hou J, Bao X. 2013. Improvement of L-arabinose fermentation by modifying the metabolic pathway and transport in Saccharomyces cerevisiae. Biomed. Res. Int. 2013:461204.
  38. Wang C, Zhao J, Qiu C, Wang S, Shen Y, Du B, et al. 2017. Coutilization of D-glucose, D-xylose, and L-arabinose in Saccharomyces cerevisiae by coexpressing the metabolic pathways and evolutionary engineering. Biomed. Res. Int. 2017: 5318232.
  39. Bettiga M, Bengtsson O, Hahn-Hagerdal B, Gorwa-Grauslund MF. 2009. Arabinose and xylose fermentation by recombinant Saccharomyces cerevisiae expressing a fungal pentose utilization pathway. Microb. Cell Fact. 8: 1-12. https://doi.org/10.1186/1475-2859-8-1
  40. Watanabe S, Utsumi Y, Sawayama S, Watanabe Y. 2016. Identification and characterization of D-arabinose reductase and D-arabinose transporters from Pichia stipitis. Biosci. Biotechnol. Biochem. 80: 2151-2158. https://doi.org/10.1080/09168451.2016.1204221
  41. Richard P, Putkonen M, Vaananen R, Londesborough J, Penttila M. 2002. The missing link in the fungal L-arabinose catabolic pathway, identification of the L-xylulose reductase gene. Biochem. 41: 6432-6437. https://doi.org/10.1021/bi025529i
  42. Metz B, de Vries RP, Polak S, Seidl V, Seiboth B. 2009. The Hypocrea jecorina (syn. Trichoderma reesei) lxr1 gene encodes a d-mannitol dehydrogenase and is not involved in Larabinose catabolism. FEBS Lett. 583: 1309-1313. https://doi.org/10.1016/j.febslet.2009.03.027
  43. Wiedemann B, Boles E. 2008. Codon-optimized bacterial genes improve L-arabinose fermentation in recombinant Saccharomyces cerevisiae. Appl. Environ. Microbiol. 74: 2043-2050. https://doi.org/10.1128/AEM.02395-07
  44. Wang X, Yang J, Yang S, Jiang Y. 2019. Unraveling the genetic basis of fast l-arabinose consumption on top of recombinant xylose-fermenting Saccharomyces cerevisiae. Biotechnol. Bioeng. 116: 283-293. https://doi.org/10.1002/bit.26827
  45. Lee DW, Hong YH, Choe EA, Lee SJ, Kim SB, Lee HS, et al. 2005. A thermodynamic study of mesophilic, thermophilic, and hyperthermophilic L-arabinose isomerases: the effects of divalent metal ions on protein stability at elevated temperatures. FEBS Lett. 579: 1261-1266. https://doi.org/10.1016/j.febslet.2005.01.027
  46. Jansen MLA, Bracher JM, Papapetridis I, Verhoeven MD, de Bruijn H, de Waal PP, et al. 2017. Saccharomyces cerevisiae strains for second-generation ethanol production: from academic exploration to industrial implementation. FEMS Yeast Res. 17: fox044. https://doi.org/10.1093/femsyr/fox044
  47. Leandro MJ, Fonseca C, Goncalves P. 2009. Hexose and pentose transport in ascomycetous yeasts: An overview. FEMS Yeast Res. 9: 511-525. https://doi.org/10.1111/j.1567-1364.2009.00509.x
  48. Subtil T, Boles E. 2011. Improving L-arabinose utilization of pentose fermenting Saccharomyces cerevisiae cells by heterologous expression of L-arabinose transporting sugar transporters. Biotechnol. Biofuels 4: 1-10. https://doi.org/10.1186/1754-6834-4-1
  49. Verhoeven MD, Bracher JM, Nijland JG, Bouwknegt J, Daran JG, Driessen AJM, et al. 2018. Laboratory evolution of a glucose-phosphorylation-deficient, arabinose-fermenting S. cerevisiae strain reveals mutations in GAL2 that enable glucose-insensitive l-arabinose uptake. FEMS Yeast Res. 18: doi: 10.1093/femsyr/foy062.
  50. Li J, Xu J, Cai P, Wang B, Ma Y, Benz JP, et al. 2015. Functional analysis of two L-arabinose transporters from filamentous fungi reveals promising characteristics for improved pentose utilization in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 81: 4062-4070. https://doi.org/10.1128/AEM.00165-15
  51. Bracher JM, Verhoeven MD, Wisselink HW, Crimi B, Nijland JG, Driessen AJM, et al. 2018. The Penicillium chrysogenum transporter Pc AraT enables high-affinity, glucose-insensitive L-arabinose transport in Saccharomyces cerevisiae. Biotechnol. Biofuels 11:63. https://doi.org/10.1186/s13068-018-1047-6
  52. Verhoeven MD, de Valk SC, Daran JG, van Maris AJA, Pronk JT. 2018. Fermentation of glucose-xylose-arabinose mixtures by a synthetic consortium of single-sugar-fermenting Saccharomyces cerevisiae strains. FEMS Yeast Res. 18: doi:10.1093/femsyr/foy075.
  53. 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: 274-282. https://doi.org/10.1016/j.tibtech.2012.01.005
  54. Lane S, Xu H, Oh EJ, Kim H, Lesmana A, Jeong D, et al. 2018. Glucose repression can be alleviated by reducing glucose phosphorylation rate in Saccharomyces cerevisiae. Sci. Rep. 8: 2613. https://doi.org/10.1038/s41598-018-20804-4
  55. Deanda K, Zhang MIN, Eddy C, Picataggio S. 1996. Development of an arabinose-fermenting Zymomonas mobilis strain by metabolic pathway engineering. Microbiol. 62: 4465-4470.
  56. Schneider J, Niermann K, Wendisch VF. 2011. Production of the amino acids L-glutamate, L-lysine, L-ornithine and Larginine from arabinose by recombinant Corynebacterium glutamicum. J. Biotechnol. 154: 191-198. https://doi.org/10.1016/j.jbiotec.2010.07.009
  57. Searchinger T, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, et al. 2008. Use of U.S. croplands for biofuels increases greenhouse gases through emissions from landuse change. Science 423: 1238-1241.
  58. Lynd LR. 2017. The grand challenge of cellulosic biofuels. Nat. Biotechnol. 35: 912-915. https://doi.org/10.1038/nbt.3976

Cited by

  1. Deletion of PHO13 improves aerobic L-arabinose fermentation in engineered Saccharomyces cerevisiae vol.46, pp.12, 2019, https://doi.org/10.1007/s10295-019-02233-y
  2. Yeast Synthetic Biology for the Production of Lycium barbarum Polysaccharides vol.26, pp.6, 2019, https://doi.org/10.3390/molecules26061641
  3. Pentose metabolism and conversion to biofuels and high-value chemicals in yeasts vol.45, pp.4, 2019, https://doi.org/10.1093/femsre/fuaa069
  4. Metagenomic Insight into Lignocellulose Degradation of the Thermophilic Microbial Consortium TMC7 vol.31, pp.8, 2019, https://doi.org/10.4014/jmb.2106.06015
  5. Functional characterization of a highly specific l-arabinose transporter from Trichoderma reesei vol.20, pp.1, 2021, https://doi.org/10.1186/s12934-021-01666-4
  6. Physiological limitations and opportunities in microbial metabolic engineering vol.20, pp.1, 2019, https://doi.org/10.1038/s41579-021-00600-0