Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 14, pp 14171–14181 | Cite as

Biodegradation of kraft lignin by newly isolated Klebsiella pneumoniae, Pseudomonas putida, and Ochrobactrum tritici strains

  • Zhaoxian Xu
  • Ling Qin
  • Mufeng Cai
  • Wenbo Hua
  • Mingjie JinEmail author
Research Article

Abstract

Bacterial systems have drawn an increasing amount of attention on lignin valorization due to their rapid growth and powerful environmental adaptability. In this study, Klebsiella pneumoniae NX-1, Pseudomonas putida NX-1, and Ochrobactrum tritici NX-1 with ligninolytic potential were isolated from leaf mold samples. Their ligninolytic capabilities were determined by measuring (1) the cell growth on kraft lignin as the sole carbon source, (2) the decolorization of kraft lignin and lignin-mimicking dyes, (3) the micro-morphology changes and transformations of chemical groups in kraft lignin, and (4) the ligninolytic enzyme activities of these three isolates. To the best of our knowledge, this is the first report that Ochrobactrum tritici species can depolymerize and metabolize lignin. Moreover, laccase, lignin peroxidase, and Mn-peroxidase showed high activities in P. putida NX-1. Due to their excellent ligninolytic capabilities, these three bacteria are important supplements to ligninolytic bacteria library and could be valuable in lignin valorization.

Keywords

Lignin Biodegradation Klebsiella pneumoniae Pseudomonas putida Ochrobactrum tritici Ligninolytic enzymes 

Notes

Acknowledgements

This work was supported by the National Key R&D Program of China (grant number 2016YFE0105400), National Natural Science Foundation of China (grant number 21606132), Natural Science Foundation of Jiangsu Province (grant numbers BK20160823 and BK20170829), and Fundamental Research Funds for the Central Universities (grant numbers 30916011202 and 30917011307).

Supplementary material

11356_2018_1633_MOESM1_ESM.docx (780 kb)
ESM 1 (DOCX 780 kb)

References

  1. Asina F, Brzonova I, Kozliak E, Kubátová A, Ji Y (2017) Microbial treatment of industrial lignin: successes, problems and challenges. Renew Sust Energ Rev 77:1179–1205CrossRefGoogle Scholar
  2. Bandounas L, Wierckx NJ, de Winde JH, Ruijssenaars HJ (2011) Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential. BMC Biotechnol 11:94CrossRefGoogle Scholar
  3. Bruijnincx PC, Rinaldi R, Weckhuysen BM (2015) Unlocking the potential of a sleeping giant: lignins as sustainable raw materials for renewable fuels, chemicals and materials. Green Chem 17:4860–4861CrossRefGoogle Scholar
  4. Bugg TD, Ahmad M, Hardiman EM, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400CrossRefGoogle Scholar
  5. Cannatelli MD, Ragauskas AJ (2016) Conversion of lignin into value-added materials and chemicals via laccase-assisted copolymerization. Appl Microbiol Biotechnol 100:8685–8691CrossRefGoogle Scholar
  6. Carles L, Rossi F, Joly M, Besse-Hoggan P, Batisson I, Artigas J (2017) Biotransformation of herbicides by aquatic microbial communities associated to submerged leaves. Environ Sci Pollut Res 24:3664–3674CrossRefGoogle Scholar
  7. Carvalho SI, Otero M, Duarte AC, Santos EB (2008) Spectroscopic changes on fulvic acids from a kraft pulp mill effluent caused by sun irradiation. Chemosphere 73:1845–1852CrossRefGoogle Scholar
  8. Chai LY, Chen YH, Tang CJ, Yang ZH, Zheng Y, Shi Y (2014) Depolymerization and decolorization of kraft lignin by bacterium Comamonas sp. B-9. Appl Microbiol Biotechnol 98:1907–1912CrossRefGoogle Scholar
  9. Chandel AK, Gonçalves BC, Strap JL, da Silva SS (2015) Biodelignification of lignocellulose substrates: an intrinsic and sustainable pretreatment strategy for clean energy production. Crit Rev Biotechnol 35:281–293CrossRefGoogle Scholar
  10. Chang YC, Choi D, Takamizawa K, Kikuchi S (2014) Isolation of Bacillus sp. strains capable of decomposing alkali lignin and their application in combination with lactic acid bacteria for enhancing cellulase performance. Bioresour Technol 152:429–436CrossRefGoogle Scholar
  11. Chen Z, Wan C (2017) Biological valorization strategies for converting lignin into fuels and chemicals. Renew Sust Energ Rev 73:610–621CrossRefGoogle Scholar
  12. 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 112:900–906CrossRefGoogle Scholar
  13. Chen Y, Huang J, Li Y, Zeng G, Zhang J, Huang A, Zhang J, Ma S, Tan X, Xu W, Zhou W (2015) Study of the rice straw biodegradation in mixed culture of Trichoderma viride and Aspergillus niger by GC-MS and FTIR. Environ Sci Pollut Res 22:9807–9815CrossRefGoogle Scholar
  14. Cohen MS, Gabriele PD (1982) Degradation of coal by the fungi Polyporus versicolor and Poria monticola. Appl Microbiol Biotechnol 44:23–27Google Scholar
  15. dos Santos TC, Zocolo GJ, Morales DA, de Aragão Umbuzeiro G, Zanoni MVB (2014) Assessment of the breakdown products of solar/UV induced photolytic degradation of food dye tartrazine. Food Chem Toxicol 68:307–315CrossRefGoogle Scholar
  16. Farag S, Chaouki J (2015) Economics evaluation for on-site pyrolysis of kraft lignin to value-added chemicals. Bioresour Technol 175:254–261CrossRefGoogle Scholar
  17. Hermosilla E, Schalchli H, Mutis A, Diez MC (2017) Combined effect of enzyme inducers and nitrate on selective lignin degradation in wheat straw by Ganoderma lobatum. Environ Sci Pollut Res 24:21984–21996.  https://doi.org/10.1007/s11356-017-9841-4 CrossRefGoogle Scholar
  18. Holladay JE, White JF, Bozell JJ, Johnson D (2007) Top value-added chemicals from biomass—volume II. Results of screening for potential candidates from biorefinery lignin (No. PNNL-16983). Pacific Northwest National Lab.(PNNL), Richland, WA (United States); National Renewable Energy Laboratory (NREL), Golden, CO (United States)Google Scholar
  19. Huang XF, Santhanam N, Badri DV, Hunter WJ, Manter DK, Decker SR, Vivanco JM, Reardon KF (2013) Isolation and characterization of lignin-degrading bacteria from rainforest soils. Biotechnol Bioeng 110:1616–1626CrossRefGoogle Scholar
  20. Humbird D, Davis R, Tao L, Kinchin C, Hsu D, Aden A (2011) Process design and economics for biochemical conversion of lignocellulosic biomass to ethanol. NREL technical report, NREL/TP-5100-47764: 1–114Google Scholar
  21. Jackson CA, Couger MB, Prabhakaran M, Ramachandriya KD, Canaan P, Fathepure BZ (2017) Isolation and characterization of Rhizobium sp. strain YS-1r that degrades lignin in plant biomass. J Appl Microbiol 122:940–952CrossRefGoogle Scholar
  22. Johnson CW, Beckham GT (2015) Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metab Eng 28:240–247CrossRefGoogle Scholar
  23. Kapich AN, Prior BA, Botha A, Galkin S, Lundell T, Hatakka A (2004) Effect of lignocellulose-containing substrates on production of ligninolytic peroxidases in submerged cultures of Phanerochaete chrysosporium ME-446. Enzym Microb Technol 34(2):187–195CrossRefGoogle Scholar
  24. Kosa M, Ragauskas AJ (2013) Lignin to lipid bioconversion by oleaginous Rhodococci. Green Chem 15:2070–2074CrossRefGoogle Scholar
  25. Koyani RD, Sanghvi GV, Sharma RK, Rajput KS (2013) Contribution of lignin degrading enzymes in decolourisation and degradation of reactive textile dyes. Int Biodeterior Biodegrad 77:1–9CrossRefGoogle Scholar
  26. Kumar M, Singh J, Singh MK, Singhal A, Thakur IS (2015) Investigating the degradation process of kraft lignin by β-proteobacterium, Pandoraea sp. ISTKB. Environ Sci Pollut Res 22:15690–15702CrossRefGoogle Scholar
  27. Li C, Zhao X, Wang A, Huber GW, Zhang T (2015) Catalytic transformation of lignin for the production of chemicals and fuels. Chem Rev 115:11559–11624CrossRefGoogle Scholar
  28. Lin L, Cheng Y, Pu Y, Sun S, Li X, Jin M, Pierson EA, Gross DC, Dale BE, Dai SY, Ragauskas AJ, Yuan JS (2016) Systems biology-guided biodesign of consolidated lignin conversion. Green Chem 18:5536–5547CrossRefGoogle Scholar
  29. Liu Y, Hu T, Wu Z, Zeng G, Huang D, Shen Y, He X, Lai M, He Y (2014) Study on biodegradation process of lignin by FTIR and DSC. Environ Sci Pollut Res 21(24):14004–14013CrossRefGoogle Scholar
  30. Mathews SL, Pawlak JJ, Grunden AM (2014) Isolation of Paenibacillus glucanolyticus from pulp mill sources with potential to deconstruct pulping waste. Bioresour Technol 164:100–105CrossRefGoogle Scholar
  31. Mathews SL, Grunden AM, Pawlak J (2016) Degradation of lignocellulose and lignin by Paenibacillus glucanolyticus. Int Biodeter Biodegr 110:79–86Google Scholar
  32. Morii H, Nakamiya K, Kinoshita S (1995) Isolation of a lignin-decolorizing bacterium. J Biosci Bioeng 80:296–299Google Scholar
  33. Paliwal R, Uniyal S, Rai JPN (2015) Evaluating the potential of immobilized bacterial consortium for black liquor biodegradation. Environ Sci Pollut Res 22:6842–6853CrossRefGoogle Scholar
  34. Patil MD, Dev MJ, Tangadpalliwar S, Patel G, Garg P, Chisti Y, Banerjee UC (2017) Ultrasonic disruption of Pseudomonas putida for the release of arginine deiminase: kinetics and predictive models. Bioresour Technol 233:74–83CrossRefGoogle Scholar
  35. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, Davison BH, Dixon RA, Gilna P, Keller M, Langan P, Naskar AK, Saddler JN, Tschaplinski TJ, Tuskan GA, Wyman CE (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 344:1246843CrossRefGoogle Scholar
  36. Raj A, Chandra R, Reddy MMK, Purohit HJ, Kapley A (2007a) Biodegradation of kraft lignin by a newly isolated bacterial strain, Aneurinibacillus aneurinilyticus from the sludge of a pulp paper mill. World J Microbiol Biotechnol 23:793–799CrossRefGoogle Scholar
  37. Raj A, Reddy MK, Chandra R, Purohit HJ, Kapley A (2007b) Biodegradation of kraft-lignin by Bacillus sp. isolated from sludge of pulp and paper mill. Biodegradation 18:783–792CrossRefGoogle Scholar
  38. Ramachandra M, Crawford DL, Hertel G (1988) Characterization of an extracellular lignin peroxidase of the lignocellulolytic actinomycete Streptomyces viridosporus. Appl Environ Microbiol 54(12):3057–3063Google Scholar
  39. Ravi K, García-Hidalgo J, Gorwa-Grauslund MF, Lidén G (2017) Conversion of lignin model compounds by Pseudomonas putida KT2440 and isolates from compost. Appl Microbiol Biotechnol 101:5059–5070CrossRefGoogle Scholar
  40. Ruijssenaars HJ, Hartmans S (2004) A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl Microbiol Biotechnol 65:177–182CrossRefGoogle Scholar
  41. Rumyantseva YI, Zhbankov RG, Marhevka R, Rataiczak H (1994) IR spectra and structure of alkaline lignin and thiolignin. J Appl Spectrosc 61:699–703CrossRefGoogle Scholar
  42. Sakamoto Y, Nakade K, Yano A, Nakagawa Y, Hirano T, Irie T, Watanabe H, Nagai M, Sato T (2008) Heterologous expression of lcc1 from Lentinula edodes in tobacco BY-2 cells results in the production an active, secreted form of fungal laccase. Appl Microbiol Biotechnol 79:971–980CrossRefGoogle Scholar
  43. Shi Y, Yan X, Li Q, Wang X, Xie S, Chai L, Yuan J (2017) Directed bioconversion of Kraft lignin to polyhydroxyalkanoate by Cupriavidus basilensis B-8 without any pretreatment. Process Biochem 52:238–242CrossRefGoogle Scholar
  44. Shields-Menard SA, AmirSadeghi M, Green M, Womack E, Sparks DL, Blake J, Edelmann M, Ding X, Sukhbaatar B, Hernandez R, Donaldson JR, French TR (2017) The effects of model aromatic lignin compounds on growth and lipid accumulation of Rhodococcus rhodochrous. Int Biodeterior Biodegrad 121:79–90CrossRefGoogle Scholar
  45. Suman SK, Dhawaria M, Tripathi D, Raturi V, Adhikari DK, Kanaujia PK (2016) Investigation of lignin biodegradation by Trabulsiella sp. isolated from termite gut. Int Biodeterior Biodegrad 112:12–17CrossRefGoogle Scholar
  46. Tian JH, Pourcher AM, Bouchez T, Gelhaye E, Peu P (2014) Occurrence of lignin degradation genotypes and phenotypes among prokaryotes. Appl Microbiol Biotechnol 98:9527–9544CrossRefGoogle Scholar
  47. Tian JH, Pourcher AM, Peu P (2016) Isolation of bacterial strains able to metabolize lignin and lignin-related compounds. Lett Appl Microbiol 63:30–37CrossRefGoogle Scholar
  48. 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 8:617–628CrossRefGoogle Scholar
  49. Wang BZ, Ma Y, Zhou WY, Zheng JW, Zhu JC, He J, Li SP (2011) Biodegradation of synthetic pyrethroids by Ochrobactrum tritici strain pyd-1. World J Microbiol Biotechnol 27:2315–2324CrossRefGoogle Scholar
  50. Wang S, Ru B, Lin H, Sun W, Luo Z (2015) Pyrolysis behaviors of four lignin polymers isolated from the same pine wood. Bioresour Technol 182:120–127CrossRefGoogle Scholar
  51. Wong PK, Yuen PY (1996) Decolorization and biodegradation of methyl red by Klebsiella pneumoniae RS-13. Water Res 30:1736–1744CrossRefGoogle Scholar
  52. Wong PK, Yuen PY (1998) Decolorization and biodegradation of N, N′-dimethyl-p-phenylenediamine by Klebsiella pneumoniae RS-13 and Acetobacter liquefaciens S-1. Lett Appl Microbiol 85:79–87CrossRefGoogle Scholar
  53. Xu H, Guo MY, Gao YH, Bai XH, Zhou XW (2017) Expression and characteristics of manganese peroxidase from Ganoderma lucidum in Pichia pastoris and its application in the degradation of four dyes and phenol. BMC Biotechnol 17:19CrossRefGoogle Scholar
  54. Yadav S, Chandra R (2015) Syntrophic co-culture of Bacillus subtilis and Klebsiella pneumonia for degradation of kraft lignin discharged from rayon grade pulp industry. J Environ Sci 33:229–238CrossRefGoogle Scholar
  55. Yu H, Tang H, Li Y, Xu P (2015) Molybdenum-containing nicotine hydroxylase genes in a nicotine degradation pathway that is a variant of the pyridine and pyrrolidine pathways. Appl Environ Microbiol 81:8330–8338CrossRefGoogle Scholar
  56. Zeng Y, Zhao S, Yang S, Ding SY (2014) Lignin plays a negative role in the biochemical process for producing lignocellulosic biofuels. Curr Opin Biotechnol 27:38–45CrossRefGoogle Scholar
  57. Zhao C, Xie S, Pu Y, Zhang R, Huang F, Ragauskas AJ, Yuan JS (2016) Synergistic enzymatic and microbial lignin conversion. Green Chem 18:1306–1312CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Zhaoxian Xu
    • 1
  • Ling Qin
    • 1
  • Mufeng Cai
    • 1
  • Wenbo Hua
    • 1
  • Mingjie Jin
    • 1
    Email author
  1. 1.School of Environmental and Biological EngineeringNanjing University of Science and TechnologyNanjingChina

Personalised recommendations