Bioconversion of lignin into bioplastics by Pandoraea sp. B-6: molecular mechanism

Abstract

Lignin is a byproduct in the pulp and paper industry and is considered as a promising alternative for the provision of energy and chemicals. Currently, the efficient valorization of lignin is a challenge owing to its polymeric structure complexity. Here, we present a platform for bio-converting Kraft lignin (KL), to polyhydroxyalkanoate (PHA) by Pandoraea sp. B-6 (hereafter B-6). Depolymerization of KL by B-6 was first confirmed, and > 40% KL was degraded by B-6 in the initial 4 days. Characterization of PHA showed that up to 24.7% of PHA accumulated in B-6 grown in 6-g/L KL mineral medium. The composition, structure, and thermal properties of the produced PHA were analyzed, revealing that 3-hydroxybutyrate was the only monomer and that PHA was comparable with the commercially available bioplastics. Moreover, the genomic analysis illustrated three core enzymatic systems for lignin depolymerization including laccases, peroxidases, and Fenton-reaction enzymes; five catabolic pathways for LDAC degradation and a gene cluster consisting of bktB, phaR, phaB, phaA, and phaC genes involved in PHA biosynthesis. Accordingly, a basic model for the process from lignin depolymerization to PHA production was constructed. Our findings provide a comprehensive perspective for lignin valorization and bio-material production from waste.

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References

  1. Betancur M, Bonelli PR, Velásquez JA, Cukierman AL (2009) Potentiality of lignin from the Kraft pulping process for removal of trace nickel from wastewater: effect of demineralisation. Bioresour Technol 100:1130–1137

    Article  CAS  Google Scholar 

  2. Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R (2011) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28:1883–1896

    Article  CAS  Google Scholar 

  3. Chai L, Chen Y, Tang C, Yang Z, Zheng Y, Shi Y (2014) Depolymerization and decolorization of Kraft lignin by bacterium Comamonas sp. B-9. Appl Microbiol Biotechnol 98:1907–1912

    Article  CAS  Google Scholar 

  4. Chen YH, Chai LY, Zhu YH, Yang ZH, Zheng Y, Zhang H (2012) Biodegradation of Kraft lignin by a bacterial strain Comamonas sp. B-9 isolated from eroded bamboo slips. J Appl Microbiol 112:900–906

    Article  CAS  Google Scholar 

  5. Ciesielczyk F, Bartczak P, Klapiszewski Ł, Jesionowski T (2017) Treatment of model and galvanic waste solutions of copper(II) ions using a lignin/inorganic oxide hybrid as an effective sorbent. J Hazard Mater 328:150–159

    Article  CAS  Google Scholar 

  6. Estrada JM, Hernández S, Muñoz R, Revah S (2013) A comparative study of fungal and bacterial biofiltration treating a VOC mixture. J Hazard Mater 250-251:190–197

    Article  CAS  Google Scholar 

  7. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martínez AT, Otillar R, Spatafora JW, Yadav JS, Aerts A, Benoit I, Boyd A, Carlson A, Copeland A, Coutinho PM, de Vries RP, Ferreira P, Findley K, Foster B, Gaskell J, Glotzer D, Górecki P, Heitman J, Hesse C, Hori C, Igarashi K, Jurgens JA, Kallen N, Kersten P, Kohler A, Kües U, Kumar TKA, Kuo A, LaButti K, Larrondo LF, Lindquist E, Ling A, Lombard V, Lucas S, Lundell T, Martin R, McLaughlin DJ, Morgenstern I, Morin E, Murat C, Nagy LG, Nolan M, Ohm RA, Patyshakuliyeva A, Rokas A, Ruiz-Dueñas FJ, Sabat G, Salamov A, Samejima M, Schmutz J, Slot JC, John FS, Stenlid J, Sun H, Sun S, Syed K, Tsang A, Wiebenga A, Young D, Pisabarro A, Eastwood DC, Martin F, Cullen D, Grigoriev IV, Hibbett DS (2012) The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

    Article  CAS  Google Scholar 

  8. Frank K, Sippl MJ (2008) High-performance signal peptide prediction based on sequence alignment techniques. Bioinformatics 24:2172–2176

    Article  CAS  Google Scholar 

  9. Haq I, Kumar S, Kumari V, Singh SK, Raj A (2016) Evaluation of bioremediation potentiality of ligninolytic Serratia liquefaciens for detoxification of pulp and paper mill effluent. J Hazard Mater 305:190–199

    Article  CAS  Google Scholar 

  10. Jimenez JR, Claiborn CS, Dhammapala RS, Simpson CD (2007) Methoxyphenols and levoglucosan ratios in PM2.5 from wheat and Kentucky bluegrass stubble burning in eastern Washington and northern Idaho. Environ Sci Technol 41:7824–7829

    Article  CAS  Google Scholar 

  11. Kong L, Hasanbeigi A, Price L (2016) Assessment of emerging energy-efficiency technologies for the pulp and paper industry: a technical review. J Clean Prod 122:5–28

    Article  CAS  Google Scholar 

  12. Kosa M, Ragauskas AJ (2013) Lignin to lipid bioconversion by oleaginous Rhodococci. Green Chem 15:2070–2074

    Article  CAS  Google Scholar 

  13. Levasseur A, Piumi F, Coutinho PM, Rancurel C, le Asther M, Delattre M, Henrissat B, Pontarotti P, Asther M, Record E (2008) FOLy: an integrated database for the classification and functional annotation of fungal oxidoreductases potentially involved in the degradation of lignin and related aromatic compounds. Fungal Genet Biol 45:638–645

    Article  CAS  Google Scholar 

  14. Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272

    Article  CAS  Google Scholar 

  15. Li J, Li Y, Wu Y, Zheng M (2014) A comparison of biochars from lignin, cellulose and wood as the sorbent to an aromatic pollutant. J Hazard Mater 280:450–457

    Article  CAS  Google Scholar 

  16. Li Z, Ge Y, Wan L (2015) Fabrication of a green porous lignin-based sphere for the removal of lead ions from aqueous media. J Hazard Mater 285:77–83

    Article  CAS  Google Scholar 

  17. Linger JG, Vardon DR, Guarnieri MT, Karp EM, Hunsinger GB, Franden MA, Johnson CW, Chupka G, Strathmann TJ, Pienkos PT, Beckham GT (2014) Lignin valorization through integrated biological funneling and chemical catalysis. Proc Natl Acad Sci USA 111:12013–12018

    Article  CAS  Google Scholar 

  18. Liu B, Jin Y, Xie G, Wang Z, Wen H, Ren N, Xing D (2018a) Simultaneous photo catalysis of SiC/Fe3O4 nano-particles and photo-fermentation of Rhodopseudomonas sp. nov. strain A7 for enhancing hydrogen production under visible light irradiation. ES Energ Environ 1:56–66

    Google Scholar 

  19. Liu D, Yan X, Zhuo S, Si M, Liu M, Wang S, Ren L, Chai L, Shi Y (2018b) Pandoraea sp. B-6 assists the deep eutectic solvent pretreatment of rice straw via promoting lignin depolymerization. Bioresour Technol 257:62–68

    Article  CAS  Google Scholar 

  20. Lourençon TV, Hansel FA, Silva TAD, Ramos LP, de Muniz GIB, Magalhães WLE (2015) Hardwood and softwood Kraft lignins fractionation by simple sequential acid precipitation. Sep Purif Technol 154:82–88

    Article  CAS  Google Scholar 

  21. Lv H, Yan L, Zhang M, Geng Z, Ren M, Sun Y (2013) Influence of supercritical CO2 pretreatment of corn stover with ethanol-water as co-solvent on lignin degradation. Chem Eng Technol 36:1899–1906

    Article  CAS  Google Scholar 

  22. Ma J, Zhang K, Liao H, Hector SB, Shi X, Li J, Liu B, Xu T, Tong C, Liu X, Zhu Y (2016) Genomic and secretomic insight into lignocellulolytic system of an endophytic bacterium Pantoea ananatis Sd-1. Biotechnol Biofuels 9:25

    Article  CAS  Google Scholar 

  23. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P, Hammel KE, Wymelenberg AV, Gaskell J, Lindquist E, Sabat G, BonDurant SS, Larrondo LF, Canessa P, Vicuna R, Yadav J, Doddapaneni H, Subramanian V, Pisabarro AG, Lavín JL, Oguiza JA, Master E, Henrissat B, Coutinho PM, Harris P, Magnuson JK, Baker SE, Bruno K, Kenealy W, Hoegger PJ, Kües U, Ramaiya P, Lucas S, Salamov A, Shapiro H, Tu H, Chee CL, Misra M, Xie G, Teter S, Yaver D, James T, Mokrejs M, Pospisek M, Grigoriev IV, Brettin T, Rokhsar D, Berka R, Cullen D (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959

    Article  Google Scholar 

  24. Masai E, Katayama Y, Fukuda M (2007) Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem 71:1–15

    Article  CAS  Google Scholar 

  25. Nakamura T, Kawamoto H, Saka S (2007) Condensation reactions of some lignin related compounds at relatively low pyrolysis temperature. J Wood Chem Technol 27:121–133

    Article  CAS  Google Scholar 

  26. Nanayakkara S, Patti AF, Saito K (2014) Lignin depolymerization with phenol via redistribution mechanism in ionic liquids. ACS Sustain Chem Eng 2:2159–2164

    Article  CAS  Google Scholar 

  27. Palmeiro-Sánchez T, Fra-Vázquez A, Rey-Martínez N, Campos JL, Mosquera-Corral A (2016) Transient concentrations of NaCl affect the PHA accumulation in mixed microbial culture. J Hazard Mater 306:332–339

    Article  CAS  Google Scholar 

  28. Pandey MP, Kim CS (2011) Lignin depolymerization and conversion: a review of thermochemical methods. Chem Eng Technol 34:29–41

    Article  CAS  Google Scholar 

  29. Pérez-Pantoja D, De la Iglesia R, Pieper DH, González B (2008) Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol Rev 32:736–794

    Article  CAS  Google Scholar 

  30. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  CAS  Google Scholar 

  31. Pfliegera M, Kroflič A (2017) Acute toxicity of emerging atmospheric pollutants from wood lignin due to biomass burning. J Hazard Mater 338:132–139

    Article  CAS  Google Scholar 

  32. Reading NS, Welch KD, Aust SD (2003) Free radical reactions of wood-degrading fungi. ACS Symposium Series No. 845. American Chemical Society, Washington, pp. 16–31

  33. Reddy MV, Yajima Y, Mawatari Y, Hoshino T, Chang Y (2015) Degradation and conversion of toxic compounds into useful bioplastics by Cupriavidus sp. CY-1: relative expression of the PhaC gene under phenol and nitrogen stress. Green Chem 17:4560–4569

    Article  CAS  Google Scholar 

  34. Reddy MV, Mawatari Y, Onodera R, Nakamura Y, Yajima Y, Chang Y (2017) Polyhydroxyalkanoates (PHA) production from synthetic waste using Pseudomonas pseudoflava: PHA synthase enzyme activity analysis from P. pseudoflava and P. palleronii. Bioresour Technol 234:99–105

    Article  CAS  Google Scholar 

  35. Rehm BHA, Steinbüchel A (1999) Biochemical and genetic analysis of PHA synthases and other proteins required for PHA synthesis. Int J Biol Macromol 25:3–19

    Article  CAS  Google Scholar 

  36. Santos OSH, Silva MCD, Silva VR, Mussel WN, Yoshida MI (2017) Polyurethane foam impregnated with lignin as a filler for the removal of crude oil from contaminated water. J Hazard Mater 324(PART B):406–413

    Article  CAS  Google Scholar 

  37. Sen S, Patil S, Argyropoulos DS (2015) Methylation of softwood Kraft lignin with dimethyl carbonate. Green Chem 17:1077–1087

    Article  CAS  Google Scholar 

  38. Shi Y, Chai L, Tang C, Yang Z, Zhang H, Chen R, Chen Y, Zheng Y (2013a) Characterization and genomic analysis of Kraft lignin biodegradation by the beta-proteobacterium Cupriavidus basilensis B-8. Biotechnol Biofuels 6(1):1

    Article  CAS  Google Scholar 

  39. Shi Y, Chai L, Tang C, Yang Z, Zheng Y, Chen Y, Jing Q (2013b, 1957) Biochemical investigation of Kraft lignin degradation by Pandoraea sp. B-6 isolated from bamboo slips. Bioprocess Biosyst Eng 36:–1965

  40. Shi Y, Yan X, Li Q, Wang X, Liu M, Xie S, Chai L, Yuan J (2017) Directed bioconversion of Kraft lignin to polyhydroxyalkanoate by Cupriavidus basilensis B-8 without any pretreatment. Process Biochem 52:238–242

    Article  CAS  Google Scholar 

  41. Slater S, Houmiel KL, Tran M, Mitsky TA, Taylor NB, Padgette SR, Gruys KJ (1998) Multiple β-ketothiolases mediate poly(β-hydroxyalkanoate) copolymer synthesis in Ralstonia eutropha. J Bacteriol 180:1979–1987

    CAS  Google Scholar 

  42. Socrates G, Socrates G (2001) Infrared and Raman characteristic group frequencies: tables and charts. John Wiley & Sons, Ltd., Chichester

    Google Scholar 

  43. Song Q, Wang F, Cai J, Wang Y, Zhang J, Yu W, Xu J (2013) Lignin depolymerization (LDP) in alcohol over nickel-based catalysts via a fragmentation-hydrogenolysis process. Energy Environ Sci 6:994–1007

    Article  CAS  Google Scholar 

  44. Tian J, Pourcher A, Bouchez T, Gelhaye E, Peu P (2014) Occurrence of lignin degradation genotypes and phenotypes among prokaryotes. Appl Microbiol Biotechnol 98:9527–9544

    Article  CAS  Google Scholar 

  45. Tribot A, Delattre C, Badel E, Dussap CG, Michaud P, Baynast HD (2018) Design of experiments for bio-based composites with lignosulfonates matrix and corn cob fibers. Ind Crop Prod 123:539–545

    Article  CAS  Google Scholar 

  46. Vardon DR, Franden MA, Johnson CW, Karp EM, Guarnieri MT, Linger JG, Salm MJ, Strathmann TJ, Beckham GT (2015) Adipic acid production from lignin. Energy Environ Sci 8:617–628

    Article  CAS  Google Scholar 

  47. Wang H, Tucker M, Ji Y (2013a) Recent development in chemical depolymerization of lignin: a review. J Appl Chem 2013:1–9

  48. Wang Y, Yang Z, Peng B, Chai L, Wu B, Wu R (2013b) Biotreatment of chromite ore processing residue by Pannonibacter phragmitetus BB. Environ Sci Pollut Res, 1-10

  49. Xu C, Arancon RAD, Labidi J, Luque R (2014) Lignin depolymerisation strategies: towards valuable chemicals and fuels. Chem Soc Rev 43:7485–7500

    Article  CAS  Google Scholar 

  50. Yan X, Li Q, Chai L, Yang B, Wang Q (2014) Formation of abiological granular sludge: a facile and bioinspired proposal for improving sludge settling performance during heavy metal wastewater treatment. Chemosphere 113:36–41

    Article  CAS  Google Scholar 

  51. Yan X, Wang Z, Zhang K, Si M, Liu M, Chai L, Liu X, Shi Y (2017) Bacteria-enhanced dilute acid pretreatment of lignocellulosic biomass. Bioresour Technol 245:419–425

    Article  CAS  Google Scholar 

  52. Zakzeski J, Bruijnincx PCA, Jongerius AL, Weckhuysen BM (2010) The catalytic valorization of lignin for the production of renewable chemicals. Chem Rev 110:3552–3599

    Article  CAS  Google Scholar 

  53. Zhang K, Si M, Liu D, Zhuo S, Liu M, Liu H, Yan X, Shi Y (2018) A bionic system with Fenton reaction and bacteria as a model for bioprocessing lignocellulosic biomass. Biotechnol Biofuels:1–14

  54. Zhao M, Zhang C, Zeng G, Huang D, Xu P, Cheng M (2015) Growth, metabolism of Phanerochaete chrysosporium and route of lignin degradation in response to cadmium stress in solid-state fermentation. Chemosphere 138:560–567

    Article  CAS  Google Scholar 

  55. Zou P, Schrempf H (2000) The heme-independent manganese-peroxidase activity depends on the presence of the C-terminal domain within the Streptomyces reticuli catalase-peroxidase CpeB. FEBS J 267:2840–2849

    CAS  Google Scholar 

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Funding

This work was supported by the National Key R&D Plan (2016YFC0403003), the National Natural Science Foundation of China (31400115, 51474102), and the China Postdoctoral Science Foundation (2017M612594).

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Correspondence to Yan Shi or Liyuan Chai.

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Responsible editor: Gerald Thouand

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Liu, D., Yan, X., Si, M. et al. Bioconversion of lignin into bioplastics by Pandoraea sp. B-6: molecular mechanism. Environ Sci Pollut Res 26, 2761–2770 (2019). https://doi.org/10.1007/s11356-018-3785-1

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Keywords

  • Lignin valorization
  • Polyhydroxyalkanoate
  • Pandoraea sp. B-6
  • Genomic analysis
  • Five catabolic pathways
  • Bio-material production