Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Enhanced 2,5-Furandicarboxylic Acid (FDCA) Production in Raoultella ornithinolytica BF60 by Manipulation of the Key Genes in FDCA Biosynthesis Pathway

  • Yuan, Haibo (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University) ;
  • Liu, Yanfeng (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University) ;
  • Lv, Xueqin (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University) ;
  • Li, Jianghua (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University) ;
  • Du, Guocheng (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University) ;
  • Shi, Zhongping (Key Laboratory of Industrial Biotechnology, Ministry of Education, Jiangnan University) ;
  • Liu, Long (Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, Jiangnan University)
  • Received : 2018.08.20
  • Accepted : 2018.09.27
  • Published : 2018.12.28
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Abstract

The compound 2,5-furandicarboxylic acid (FDCA), an important bio-based monomer for the production of various polymers, can be obtained from 5-hydroxymethylfurfural (HMF). However, efficient production of FDCA from HMF via biocatalysis has not been well studied. In this study, we report the identification of key genes that are involved in FDCA synthesis and then the engineering of Raoultella ornithinolytica BF60 for biocatalytic oxidation of HMF to FDCA using its resting cells. Specifically, previously unknown candidate genes, adhP3 and alkR, which were responsible for the reduction of HMF to the undesired product 2,5-bis(hydroxymethyl)furan (HMF alcohol), were identified by transcriptomic analysis. Combinatorial deletion of these two genes resulted in 85.7% reduction in HMF alcohol formation and 23.7% improvement in FDCA production (242.0 mM). Subsequently, an aldehyde dehydrogenase, AldH, which was responsible for the oxidation of the intermediate 5-formyl-2-furoic acid (FFA) to FDCA, was identified and characterized. Finally, FDCA production was further improved by overexpressing AldH, resulting in a 96.2% yield of 264.7 mM FDCA. Importantly, the identification of these key genes not only contributes to our understanding of the FDCA synthesis pathway in R. ornithinolytica BF60 but also allows for improved FDCA production efficiency. Moreover, this work is likely to provide a valuable reference for producing other furanic chemicals.

Keywords

References

  1. Zhou C-H, Xia X, Lin C-X, Tong D-S, Beltramini J. 2011. Catalytic conversion of lignocellulosic biomass to fine chemicals and fuels. Chem. Soc. Rev. 40: 5588-5617. https://doi.org/10.1039/c1cs15124j
  2. Teong SP, Yi G, Zhang Y. 2014. Hydroxymethylfurfural production from bioresources: past, present and future. Green Chem. 16: 2015-2026. https://doi.org/10.1039/c3gc42018c
  3. Mika LT, Csefalvay E, Nemeth A. 2018. Catalytic Conversion of Carbohydrates to Initial Platform Chemicals: Chemistry and Sustainability. Chem. Rev. 118: 505-613. https://doi.org/10.1021/acs.chemrev.7b00395
  4. Sousa AF, Vilela C, Fonseca AC, Matos M, Freire CSR, Gruter G-JM, et al. 2015. Biobased polyesters and other polymers from 2,5-furandicarboxylic acid: a tribute to furan excellency. Polym. Chem. 6: 5961-5983. https://doi.org/10.1039/C5PY00686D
  5. Vilela C, Sousa AF, Fonseca AC, Serra AC, Coelho JFJ, Freire CSR, et al. 2014. The quest for sustainable polyesters-insights into the future. Polym. Chem. 5: 3119-3141. https://doi.org/10.1039/C3PY01213A
  6. Zhang Z, Deng K. 2015. Recent advances in the catalytic synthesis of 2,5-furandicarboxylic acid and its derivatives. ACS Catal. 5: 6529-6544. https://doi.org/10.1021/acscatal.5b01491
  7. Wang K-F, Liu C-l, Sui K-y, Guo C, Liu C-Z. 2018. Efficient catalytic oxidation of 5-hydroxymethylfurfural to 2,5-furandicarboxylic acid by magnetic laccase catalyst. Chembiochem. 19: 654-659. https://doi.org/10.1002/cbic.201800008
  8. Han X, Li C, Liu X, Xia Q, Wang Y. 2017. Selective oxidation of 5-hydroxymethylfurfural to 2,5-furandicarboxylic acid over MnOx-Ce$O_2$ composite catalysts. Green Chem. 19: 996-1004. https://doi.org/10.1039/C6GC03304K
  9. Xu S, Zhou P, Zhang Z, Yang C, Zhang B, Deng K, et al. 2017. Selective oxidation of 5-hydroxymethylfurfural to 2,5-furandicarboxylic acid using $O_2$ and a photocatalyst of cothioporphyrazine bonded to g-$C_3N_4$. J. Am. Chem. Soc. 139: 14775-14782. https://doi.org/10.1021/jacs.7b08861
  10. Nam D-H, Taitt BJ, Choi K-S. 2018. Copper-based catalytic anodes to produce 2,5-furandicarboxylic acid, a biomassderived alternative to terephthalic acid. ACS Catal. 8: 1197-1206. https://doi.org/10.1021/acscatal.7b03152
  11. Nestl BM, Hammer SC, Nebel BA, Hauer B. 2014. New generation of biocatalysts for organic synthesis. Angew. Chem. Int. Ed. 53: 3070-3095. https://doi.org/10.1002/anie.201302195
  12. Karich A, Kleeberg SB, Ullrich R, Hofrichter M. 2018. Enzymatic preparation of 2,5-furandicarboxylic acid (FDCA)-a substitute of terephthalic acid-by the joined action of three fungal enzymes. Microorganisms 6: 5. https://doi.org/10.3390/microorganisms6010005
  13. McKenna SM, Mines P, Law P, Kovacs-Schreiner K, Birmingham WR, Turner NJ, et al. 2017. The continuous oxidation of HMF to FDCA and the immobilisation and stabilisation of periplasmic aldehyde oxidase (PaoABC). Green Chem. 19: 4660-4665. https://doi.org/10.1039/C7GC01696D
  14. McKenna SM, Leimkuhler S, Herter S, Turner NJ, Carnell AJ. 2015. Enzyme cascade reactions: synthesis of furandicarboxylic acid (FDCA) and carboxylic acids using oxidases in tandem. Green Chem. 17: 3271-3275. https://doi.org/10.1039/C5GC00707K
  15. Carro J, Ferreira P, Rodriguez L, Prieto A, Serrano A, Balcells B, et al. 2015. 5-hydroxymethylfurfural conversion by fungal aryl-alcohol oxidase and unspecific peroxygenase. FEBS J. 282: 3218-3229. https://doi.org/10.1111/febs.13177
  16. Dijkman WP, Groothuis DE, Fraaije MW. 2014. Enzymecatalyzed oxidation of 5-hydroxymethylfurfural to furan-2,5-dicarboxylic acid. Angew. Chem. Int. Ed. 53: 6515-6518. https://doi.org/10.1002/anie.201402904
  17. Wachtmeister J, Rother D. 2016. Recent advances in whole cell biocatalysis techniques bridging from investigative to industrial scale. Curr. Opin. Biotechnol. 42: 169-177. https://doi.org/10.1016/j.copbio.2016.05.005
  18. Ladkau N, Schmid A, Buhler B. 2014. The microbial cell-functional unit for energy dependent multistep biocatalysis. Curr. Opin. Biotechnol. 30: 178-189. https://doi.org/10.1016/j.copbio.2014.06.003
  19. Schrewe M, Julsing MK, Buhler B, Schmid A. 2013. Wholecell biocatalysis for selective and productive C-O functional group introduction and modification. Chem. Soc. Rev. 42: 6346-6377. https://doi.org/10.1039/c3cs60011d
  20. Koopman F, Wierckx N, de Winde JH, Ruijssenaars HJ. 2010. Efficient whole-cell biotransformation of 5-(hydroxymethyl) furfural into FDCA, 2,5-furandicarboxylic acid. Bioresour. Technol. 101: 6291-6296. https://doi.org/10.1016/j.biortech.2010.03.050
  21. Hossain GS, Yuan H, Li J, Shin H-d, Wang M, Du G, et al. 2017. Metabolic engineering of Raoultella ornithinolytica BF60 for production of 2,5-furandicarboxylic acid from 5-hydroxymethylfurfural. Appl. Environ. Microbiol. 83: e02312-02316.
  22. Drancourt M, Bollet C, Carta A, Rousselier P. 2001. Phylogenetic analyses of Klebsiella species delineate Klebsiella and Raoultella gen. nov., with description of Raoultella ornithinolytica comb. nov., Raoultella terrigena comb. nov. and Raoultella planticola comb. nov. Int. J. Syst. Evol. Microbiol. 51: 925-932. https://doi.org/10.1099/00207713-51-3-925
  23. Sun F, Yin Z, Feng J, Qiu Y, Zhang D, Luo W, et al. 2015. Production of plasmid-encoding NDM-1 in clinical Raoultella ornithinolytica and Leclercia adecarboxylata from China. Front. Microbiol. 6: 458.
  24. Haruki Y, Hagiya H, Sakuma A, Murase T, Sugiyama T, Kondo S. 2014. Clinical characteristics of Raoultella ornithinolytica bacteremia: A case series and literature review. J. Infect. Chemother. 20: 589-591. https://doi.org/10.1016/j.jiac.2014.05.005
  25. Solak Y, Gul EE, Atalay H, Genc N, Tonbul HZ. 2011. A rare human infection of Raoultella ornithinolytica in a diabetic foot lesion. Ann. Saudi. Med. 31: 93-94. https://doi.org/10.4103/0256-4947.75794
  26. Kim T, Cho S, Lee S-M, Woo HM, Lee J, Um Y, et al. 2016. High production of 2,3-butanediol (2,3-BD) by Raoultella ornithinolytica B6 via optimizing fermentation conditions and overexpressing 2,3-BD synthesis genes. PLoS One 11: e0165076. https://doi.org/10.1371/journal.pone.0165076
  27. Hii LS, Rosfarizan M, Ling TC, Ariff AB. 2012. Statistical optimization of pullulanase production by Raoultella planticola DSMZ 4 617 using sago starch as carbon and peptone as nitrogen sources. Food Bioproc. Tech. 5: 729-737. https://doi.org/10.1007/s11947-010-0368-7
  28. Fiolka MJ, Grzywnowicz K, Rzymowska J, Lewtak K, Szewczyk R, Mendyk E, et al. 2015. Antitumour and apoptotic effects of a novel Tris-peptide complex obtained after isolation of Raoultella ornithinolytica extracellular metabolites. J. Appl. Microbiol. 118: 1357-1369. https://doi.org/10.1111/jam.12806
  29. Fiolka MJ, Lewtak K, Rzymowska J, Grzywnowicz K, Hulas-Stasiak M, Sofinska-Chmiel W, et al. 2013. Antifungal and anticancer effects of a polysaccharide-protein complex from the gut bacterium Raoultella ornithinolytica isolated from the earthworm Dendrobaena veneta. Pathog. Dis. 69: 49-61.
  30. Yuan H, Liu Y, Li J, Shin H-d, Du G, Shi Z, et al. 2018. Combinatorial synthetic pathway fine-tuning and comparative transcriptomics for metabolic engineering of Raoultella ornithinolytica BF60 to efficiently synthesize 2,5-furandicarboxylic acid. Biotechnol. Bioeng. 115: 2148-2155. https://doi.org/10.1002/bit.26725
  31. Yuan H, Li J, Shin H-d, Du G, Chen J, Shi Z, et al. 2018. Improved production of 2,5-furandicarboxylic acid by overexpression of 5-hydroxymethylfurfural oxidase and 5-hydroxymethylfurfural/furfural oxidoreductase in Raoultella ornithinolytica BF60. Bioresour. Technol. 247: 1184-1188. https://doi.org/10.1016/j.biortech.2017.08.166
  32. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97: 6640-6645. https://doi.org/10.1073/pnas.120163297
  33. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  34. Koopman F, Wierckx N, de Winde JH, Ruijssenaars HJ. 2010. Identification and characterization of the furfural and 5-(hydroxymethyl)furfural degradation pathways of Cupriavidus basilensis HMF14. Proc. Natl. Acad. Sci. USA 107: 4919-4924. https://doi.org/10.1073/pnas.0913039107
  35. Wierckx N, Koopman F, Ruijssenaars HJ, de Winde JH. 2011. Microbial degradation of furanic compounds: biochemistry, genetics, and impact. Appl. Microbiol. Biotechnol. 92: 1095-1105. https://doi.org/10.1007/s00253-011-3632-5
  36. Ishida Y, Nguyen TTM, Izawa S. 2017. The yeast ADH7 promoter enables gene expression under pronounced translation repression caused by the combined stress of vanillin, furfural, and 5-hydroxymethylfurfural. J. Biotechnol. 252: 65-72. https://doi.org/10.1016/j.jbiotec.2017.04.024
  37. Song H-S, Jeon J-M, Choi YK, Kim J-Y, Kim W, Yoon J-J, et al. 2017. L-Glycine alleviates furfural-induced growth inhibition during isobutanol production in Escherichia coli. J. Microbiol. Biotechnol. 27: 2165-2172. https://doi.org/10.4014/jmb.1705.05020
  38. Wang X, Gao Q, Bao J. 2015. Transcriptional analysis of Amorphotheca resinae ZN1 on biological degradation of furfural and 5-hydroxymethylfurfural derived from lignocellulose pretreatment. Biotechnol. Biofuels. 8: 136. https://doi.org/10.1186/s13068-015-0323-y
  39. Tsuge Y, Hori Y, Kudou M, Ishii J, Hasunuma T, Kondo A. 2014. Detoxification of furfural in Corynebacterium glutamicum under aerobic and anaerobic conditions. Appl. Microbiol. Biotechnol. 98: 8675-8683. https://doi.org/10.1007/s00253-014-5924-z
  40. Li Q, Metthew Lam LK, Xun L. 2011. Cupriavidus necator JMP134 rapidly reduces furfural with a Zn-dependent alcohol dehydrogenase. Biodegradation 22: 1215-1225. https://doi.org/10.1007/s10532-011-9476-y
  41. Yi X, Gu H, Gao Q, Liu ZL, Bao J. 2015. Transcriptome analysis of Zymomonas mobilis ZM4 reveals mechanisms of tolerance and detoxification of phenolic aldehyde inhibitors from lignocellulose pretreatment. Biotechnol. Biofuels 8: 153. https://doi.org/10.1186/s13068-015-0333-9
  42. Xu Z-H, Cheng A-D, Xing X-P, Zong M-H, Bai Y-P, Li N. 2018. Improved synthesis of 2,5-bis(hydroxymethyl)furan from 5-hydroxymethylfurfural using acclimatized whole cells entrapped in calcium alginate. Bioresour. Technol. 262: 177-183. https://doi.org/10.1016/j.biortech.2018.04.077
  43. Koma D, Yamanaka H, Moriyoshi K, Ohmoto T, Sakai K. 2012. Production of aromatic compounds by metabolically engineered Escherichia coli with an expanded shikimate pathway. Appl. Environ. Microbiol. 78: 6203-6216. https://doi.org/10.1128/AEM.01148-12
  44. Miller EN, Jarboe LR, Yomano LP, York SW, Shanmugam KT, Ingram LO. 2009. Silencing of NADPH-dependent oxidoreductase genes (yqhD and dkgA) in furfural-resistant ethanologenic Escherichia coli. Appl. Environ. Microbiol. 75: 4315-4323. https://doi.org/10.1128/AEM.00567-09

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