Conversion of lignin model compounds by Pseudomonas putida KT2440 and isolates from compost

Applied Microbiology and Biotechnology

Volumn 101, Issue 12, 2017, Pages 5059-5070

  Ravi, Krithika ^a   García Hidalgo, Javier ^a   Gorwa Grauslund, Marie F ^a   Lidén, Gunnar ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Aromatic compound conversion; Bacterial metabolism; Compost; Lignin; Pseudomonas

Indexed keywords

AROMATIC COMPOUNDS; AROMATIZATION; COMPOSTING; LIGNIN; METABOLISM; MIXTURES; PHYSIOLOGY;

16S RIBOSOMAL RNA IDENTIFICATIONS; AROMATIC MOLECULES; BACTERIAL METABOLISM; CULTURE COLLECTION; LIGNIN MODEL COMPOUND; PSEUDOMONAS; PSEUDOMONAS PUTIDA; SPECIFIC GROWTH RATE;

BACTERIA;

4 HYDROXYBENZOIC ACID; BENZOIC ACID; FERULIC ACID; LIGNIN; PARA COUMARIC ACID; RNA 16S; VANILLIC ACID; VANILLIN; 4 HYDROXYBENZOIC ACID ESTER; 4-HYDROXYBENZOIC ACID; BACTERIAL PROTEIN; BENZALDEHYDE DERIVATIVE; BENZOIC ACID DERIVATIVE; COUMARIC ACID;

BACTERIUM; COMPOST; GROWTH RATE; LIGNIN; METABOLISM; MICROBIAL ACTIVITY; NUMERICAL MODEL; ORGANIC COMPOUND;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; BIOMASS CONVERSION; CARBON SOURCE; COMPOST; CONTROLLED STUDY; GROWTH CURVE; GROWTH RATE; NONHUMAN; NUCLEOTIDE SEQUENCE; PSEUDOMONAS PUTIDA; VEGETABLE; BACTERIAL GENE; CHEMISTRY; COMPOSTING; CULTURE MEDIUM; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

AROMATIC COMPOUNDS; BACTERIA; COMPOSTING; LIGNINS; METABOLISM;

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS PUTIDA;

BACTERIAL PROTEINS; BENZALDEHYDES; BENZOATES; COMPOSTING; COUMARIC ACIDS; CULTURE MEDIA; GENES, BACTERIAL; LIGNIN; PARABENS; PSEUDOMONAS PUTIDA; RNA, RIBOSOMAL, 16S;

EID: 85015209095     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-017-8211-y     Document Type: Article

References (52)

1. Abdelaziz OY, Brink DP, Prothmann J, Ravi K, Sun M, García-Hidalgo J, Sandahl M, Hulteberg CP, Turner C, Lidén G, Gorwa-Grauslund MF (2016) Biological valorization of low molecular weight lignin. Biotechnol Adv 34(8):1318–1346. doi:10.1016/j.biotechadv.2016.10.001
2. Ahmad M, Roberts JN, Hardiman EM, Singh R, Eltis LD, Bugg TD (2011) Identification of DypB from Rhodococcus jostii RHA1 as a lignin peroxidase. Biochemistry 50(23):5096–5107. doi:10.1021/bi101892z
3. Ayyachamy M, Cliffe FE, Coyne JM, Collier J, Tuohy MG (2013) Lignin: untapped biopolymers in biomass conversion technologies. Biomass Convers Biorefin 3(3):255–269. doi:10.1007/s13399-013-0084-4
4. Beckham GT, Johnson CW, Karp EM, Salvachúa D, Vardon DR (2016) Opportunities and challenges in biological lignin valorization. Curr Opin Biotechnol 42:40–53. doi:10.1016/j.copbio.2016.02.030
5. Belda E, van Heck RG, Lopez-Sanchez MJ, Cruveiller S, Barbe V, Fraser C, Klenk HP, Petersen J, Morgat A, Nikel PI, Vallenet D, Rouy Z, Sekowska A, Martins Dos Santos VA, de Lorenzo V, Danchin A, Médigue C (2016) The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis. Environ Microbiol 18(10):3403–3424. doi:10.1111/1462-2920.13230
6. Bugg TD, Ahmad M, Hardiman EM, Rahmanpour R (2011a) Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep 28(12):1883–1896. doi:10.1039/c1np00042j
7. Bugg TD, Ahmad M, Hardiman EM, Singh R (2011b) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22(3):394–400. doi:10.1016/j.copbio.2010.10.009
8. Camarero S, Martínez MJ, Martínez AT (2014) Understanding lignin biodegradation for the improved utilization of plant biomass in modern biorefineries. Biofuels Bioprod Biorefin 8(5):615–625. doi:10.1002/bbb.1467
9. Chakar FS, Ragauskas AJ (2004) Review of current and future softwood kraft lignin process chemistry. Ind Crop Prod 20(2):131–141. doi:10.1016/j.indcrop.2004.04.016
10. 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(5):900–906. doi:10.1111/j.1365-2672.2012.05275.x
11. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2013) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42(D1):D633–D642
12. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol 9(11):803–816. doi:10.1038/nrmicro2652
13. Harwood CS, Nichols NN, Kim MK, Ditty JL, Parales RE (1994) Identification of the pcaRKF gene cluster from Pseudomonas putida: involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J Bacteriol 176(21):6479–6488
14. 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(6):1616–1626. doi:10.1002/bit.24833
15. Jiménez JI, Miñambres B, García JL, Díaz E (2002) Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4(12):824–841
16. Johnson CW, Beckham GT (2015) Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metab Eng 28:240–247. doi:10.1016/j.ymben.2015.01.005
17. Kim YH, Cho K, Yun SH, Kim JY, Kwon KH, Yoo JS, Kim SI (2006) Analysis of aromatic catabolic pathways in Pseudomonas putida KT 2440 using a combined proteomic approach: 2-DE/MS and cleavable isotope-coded affinity tag analysis. Proteomics 6(4):1301–1318. doi:10.1002/pmic.200500329
18. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62(3):716–721. doi:10.1099/ijs.0.038075-0
19. Kosa M, Ragauskas AJ (2012) Bioconversion of lignin model compounds with oleaginous Rhodococci. Appl Microbiol Biotechnol 93(2):891–900. doi:10.1007/s00253-011-3743-z
20. 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 U S A 111(33):12013–12018. doi:10.1073/pnas.1410657111
21. de Lorenzo V (2008) Systems biology approaches to bioremediation. Curr Opin Biotechnol 19(6):579–589. doi:10.1016/j.copbio.2008.10.004
22. Martín M, Gibello A, Fernández J, Ferrer E, Garrido-Pertierra A (1991) Catabolism of 3- and 4-hydroxyphenylacetic acid by Klebsiella pneumoniae. J Gen Microbiol 137(3):621–628. doi:10.1099/00221287-137-3-621
23. Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8(3):195–204
24. Martínez-García E, Nikel PI, Aparicio T, de Lorenzo V (2014) Pseudomonas 2.0: genetic upgrading of P. putida KT2440 as an enhanced host for heterologous gene expression. Microb Cell Factories 13:159. doi:10.1186/s12934-014-0159-3
25. Masai E, Katayama Y, Fukuda M (2014) Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem 71(1):1–15. doi:10.1271/bbb.60437
26. Nelson KE, Weinel C, Paulsen IT, Dodson RJ, Hilbert H, Martins dos Santos VA, Fouts DE, Gill SR, Pop M, Holmes M, Brinkac L, Beanan M, DeBoy RT, Daugherty S, Kolonay J, Madupu R, Nelson W, White O, Peterson J, Khouri H, Hance I, Chris Lee P, Holtzapple E, Scanlan D, Tran K, Moazzez A, Utterback T, Rizzo M, Lee K, Kosack D, Moestl D, Wedler H, Lauber J, Stjepandic D, Hoheisel J, Straetz M, Heim S, Kiewitz C, Eisen JA, Timmis KN, Dusterhoft A, Tummler B, Fraser CM (2002) Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ Microbiol 4(12):799–808
27. Nguyen TT, Iwaki A, Izawa S (2015) The ADH7 promoter of Saccharomyces cerevisiae is vanillin-inducible and enables mRNA translation under severe vanillin stress. Front Microbiol 6:1390. doi:10.3389/fmicb.2015.01390
28. Nikel PI, Martínez-García E, de Lorenzo V (2014) Biotechnological domestication of pseudomonads using synthetic biology. Nat Rev Microbiol 12(5):368–379. doi:10.1038/nrmicro3253
29. Nishikawa NK, Sutcliffe R, Saddler JN (1988) The influence of lignin degradation products on xylose fermentation by Klebsiella pneumoniae. Appl Microbiol Biotechnol 27(5):549–552. doi:10.1007/bf00451630
30. Okamura-Abe Y, Abe T, Nishimura K, Kawata Y, Sato-Izawa K, Otsuka Y, Nakamura M, Kajita S, Masai E, Sonoki T, Katayama Y (2016) β-ketoadipic acid and muconolactone production from a lignin-related aromatic compound through the protocatechuate 3,4-metabolic pathway. J Biosci Bioeng 121(6):652–658. doi:10.1016/j.jbiosc.2015.11.007
31. Oliva JM, Ballesteros I, Negro MJ, Manzanares P, Cabañas A, Ballesteros M (2004) Effect of binary combinations of selected toxic compounds on growth and fermentation of Kluyveromyces marxianus. Biotechnol Prog 20(3):715–720. doi:10.1021/bp034317p
32. Pérez-Pantoja D, Donoso R, Agullo L, Cordova M, Seeger M, Pieper DH, González B (2012) Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14(5):1091–1117. doi:10.1111/j.1462-2920.2011.02613.x
33. Pfennig N, Lippert KD (1966) Über das Vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch Mikrobiol 55(3):245–256. doi:10.1007/bf00410246
34. Poblete-Castro I, Becker J, Dohnt K, dos Santos VM, Wittmann C (2012) Industrial biotechnology of Pseudomonas putida and related species. Appl Microbiol Biotechnol 93(6):2279–2290. doi:10.1007/s00253-012-3928-0
35. Puchalka J, Oberhardt MA, Godinho M, Bielecka A, Regenhardt D, Timmis KN, Papin JA, Martins dos Santos VA (2008) Genome-scale reconstruction and analysis of the Pseudomonas putida KT2440 metabolic network facilitates applications in biotechnology. PLoS Comput Biol 4(10):e1000210. doi:10.1371/journal.pcbi.1000210
36. 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(6185):1246843. doi:10.1126/science.1246843
37. Raj A, Chandra R, Reddy MMK, Purohit HJ, Kapley A (2007) 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(6):793–799. doi:10.1007/s11274-006-9299-x
38. Rinaldi R, Jastrzebski R, Clough MT, Ralph J, Kennema M, Bruijnincx PCA, Weckhuysen BM (2016) Paving the way for lignin valorisation: recent advances in bioengineering, biorefining and catalysis. Angew Chem Int Ed 55(29):8164–8215. doi:10.1002/anie.201510351
39. Salvachúa D, Karp EM, Nimlos CT, Vardon DR, Beckham GT (2015) Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria. Green Chem 17(11):4951–4967. doi:10.1039/c5gc01165e
40. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual. 2001. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
41. Schwarz M, Rodríguez MC, Guillén DA, Barroso CG (2009) Development and validation of UPLC for the determination of phenolic compounds and furanic derivatives in Brandy de Jerez. J Sep Sci 32(11):1782–1790. doi:10.1002/jssc.200800706
42. Simon O, Klaiber I, Huber A, Pfannstiel J (2014) Comprehensive proteome analysis of the response of Pseudomonas putida KT2440 to the flavor compound vanillin. J Proteome 109:212–227. doi:10.1016/j.jprot.2014.07.006
43. Sudarsan S, Blank LM, Dietrich A, Vielhauer O, Takors R, Schmid A, Reuss M (2016) Dynamics of benzoate metabolism in Pseudomonas putida KT2440. Metab Eng Commun 3:97–110. doi:10.1016/j.meteno.2016.03.005
44. 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 Biodegradation 112:12–17. doi:10.1016/j.ibiod.2016.04.036
45. Sun Z, Ramsay JA, Guay M, Ramsay BA (2007) Carbon-limited fed-batch production of medium-chain-length polyhydroxyalkanoates from nonanoic acid by Pseudomonas putida KT2440. Appl Microbiol Biotechnol 74(1):69–77. doi:10.1007/s00253-006-0655-4
46. Taylor CR, Hardiman EM, Ahmad M, Sainsbury PD, Norris PR, Bugg TD (2012) Isolation of bacterial strains able to metabolize lignin from screening of environmental samples. J Appl Microbiol 113(3):521–530. doi:10.1111/j.1365-2672.2012.05352.x
47. Tuomela M, Vikman M, Hatakka A, Itävaara M (2000) Biodegradation of lignin in a compost environment: a review. Bioresour Technol 72(2):169–183. doi:10.1016/S0960-8524(99)00104-2
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(2):617–628. doi:10.1039/c4ee03230f
49. Wackett LP (2003) Pseudomonas putida—a versatile biocatalyst. Nat Biotechnol 21(2):136–138. doi:10.1038/nbt0203-136
50. Wei Z, Zeng G, Huang F, Kosa M, Huang D, Ragauskas AJ (2015) Bioconversion of oxygen-pretreated kraft lignin to microbial lipid with oleaginous Rhodococcus opacus DSM 1069. Green Chem 17(5):2784–2789. doi:10.1039/c5gc00422e
51. Woo HL, Ballor NR, Hazen TC, Fortney JL, Simmons B, Davenport KW, Goodwin L, Ivanova N, Kyrpides NC, Mavromatis K, Woyke T, Jansson J, Kimbrel J, DeAngelis KM (2014) Complete genome sequence of the lignin-degrading bacterium Klebsiella sp. strain BRL6-2. Stand Genomic Sci 9:19. doi:10.1186/1944-3277-9-19
52. Xu C, Arancon RAD, Labidi J, Luque R (2014) Lignin depolymerisation strategies: towards valuable chemicals and fuels. Chem Soc Rev 43(22):7485–7500. doi:10.1039/C4CS00235K