Genomic analysis of Burkholderia sp. ISTR5 for biofunneling of lignin-derived compounds

Biotechnology for Biofuels - Tập 12 Số 1 - 2019
Raj Morya1, Madan Kumar1, Shashi Shekhar Singh1, Indu Shekhar Thakur1
1School of Environmental Sciences, Jawaharlal Nehru University, New Delhi 110067, India

Tóm tắt

Abstract Background Lignin is the second most abundant natural polymer on earth. Industries using lignocellulosic biomass as feedstock generate a considerable amount of lignin as a byproduct with minimal usage. For a sustainable biorefinery, the lignin must be utilized in improved ways. Lignin is recalcitrant to degradation due to the complex and heterogeneous structure. The depolymerization of lignin and its conversion into specific product stream are the major challenges associated with lignin valorization. The blend of oligomeric, dimeric and monomeric lignin-derived compounds (LDCs) generated during depolymerization can be utilized by microbes for production of bioproducts. Results In the present study, a novel bacterium Burkholderia sp. strain ISTR5 (R5), a proteobacteria belonging to class betaproteobacteria, order Burkholderiales and family Burkholderiaceae, was isolated and characterized for the degradation of LDCs. R5 strain was cultured on 12 LDCs in mineral salt medium (MSM) supplemented with individual compounds such as syringic acid, p-coumaric acid, ferulic acid, vanillin, vanillic acid, guaiacol, 4-hydroxybenzoic acid, gallic acid, benzoic acid, syringaldehyde, veratryl alcohol and catechol. R5 was able to grow and utilize all the selected LDCs. The degradation of selected LDCs was monitored by bacterial growth, total organic carbon (TOC) removal and UV–Vis absorption spectra in scan mode. TOC reduction shown in the sample contains syringic acid 80.7%, ferulic acid 84.1%, p-coumaric acid 85.9% and benzoic acid 83.2%. In UV–Vis absorption spectral scan, most of the lignin-associated peaks were found at or near 280 nm wavelength in the obtained absorption spectra. Enzyme assay for the ligninolytic enzymes was also performed, and it was observed that lignin peroxidase and laccase were predominantly expressed. Furthermore, the GC–MS analysis of LDCs was performed to identify the degradation intermediates from these compounds. The genomic analysis showed the robustness of this strain and identified various candidate genes responsible for the degradation of aromatic or lignin derivatives, detoxification mechanism, oxidative stress response and fatty acid synthesis. The presence of peroxidases (13%), laccases (4%), monooxygenases (23%), dioxygenase (44%), NADPH: quinone oxidoreductases (16%) and many other related enzymes supported the degradation of LDCs. Conclusion Numerous pathway intermediates were observed during experiment. Vanillin was found during growth on syringic acid, ferulic acid and p-coumaric acid. Some other intermediates like catechol, acetovanillone, syringaldehyde and 3,4-dihydroxybenzaldehyde from the recognized bacterial metabolic pathways existed during growth on the LDCs. The ortho- and meta cleavage pathway enzymes, such as the catechol-1,2-dioxygenase, protocatechuate 3,4-dioxygenase, catechol-2,3-dioxygenase and toluene-2,3-dioxygenase, were observed in the genome. In addition to the common aromatic degradation pathways, presence of the epoxyqueuosine reductase, 1,2-epoxyphenylacetyl-CoA isomerase in the genome advocates that this strain may follow the epoxy Coenzyme A thioester pathway for degradation.

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Tài liệu tham khảo

Bibra M, Kunreddy VR, Sani RK. Thermostable xylanase production by Geobacillus sp. strain DUSELR13, and its application in ethanol production with lignocellulosic biomass. Microorganisms. 2018;6:93.

Anwar Z, Gulfraz M, Irshad M. Agro-industrial lignocellulosic biomass a key to unlock the future bio-energy, a brief review. J Radiat Res Appl Sci. 2014;7(2):163–73.

Ravi K, García-Hidalgo J, Nobel M, et al. Biological conversion of aromatic monolignol compounds by a Pseudomonas isolate from sediments of the Baltic Sea. AMB Express. 2018;32:8.

Kumar M, Singhal A, Thakur IS. Comparison of submerged and solid state pretreatment of sugarcane bagasse by Pandoraea sp. ISTKB: enzymatic and structural analysis. Bioresour Technol. 2016;203:18–25.

Thakur IS. Screening of microorganisms for removal of colour and adsorbable organic halogens from pulp and paper mill effluent. Process Biochem. 2004;39:1693–9.

Yew GY, Lee SY, Show PL, Tao Y, et al. Recent advances in algae biodiesel production: from upstream cultivation to downstream processing. Bioresour Technol Rep. 2019;7:100227.

Jonsson LJ, Alriksson B, Nilvebrant NO. Bioconversion of lignocellulose, inhibitors and detoxification. Biotechnol Biofuels. 2013;6:16.

Sierra-Alvarez R, Lettinga G. The methanogenic toxicity of wastewater lignins and lignin related compounds. J Chem Technol Biotechnol. 1991;50:443–55.

Rana BK, Johri BN, Thakur IS. Studies on formation and activities of xylan hydrolysing enzymes of Humicola grisea var thermoidea. World J Microbiol Biotechnol. 1996;12(1):12–5.

Mishra M, Thakur IS. Isolation and characterization of alkalotolerant bacteria and optimization of process parameters for decolorization and detoxification of pulp and paper mill effluent by Taguchi approach. Biodegradation. 2010;21:967–78.

Wang J, Liang J, Gao S. Biodegradation of lignin monomers vanillic, p-coumaric, and syringic acid by the bacterial strain, Sphingobacterium sp. HY-H. Curr Microbiol. 2018;75:1156.

Adetitun D, Fatehpure B, Hugh H, et al. Degradation of hydrocarbons and lignin-like compounds by Alcaligens sp. strain 3 k isolated from Ilorin. Pollution. 2019;5(2):269–77.

Nishimura M, Ooi O, Davies J. Isolation and characterization of Streptomyces sp. NL15-2K capable of degrading lignin-related aromatic compounds. J Biosci Bioeng. 2006;102(2):124–7.

Tomizawa S, Chuah JA, Matsumoto K, et al. Understanding the limitations in the biosynthesis of polyhydroxyalkanoate (PHA) from lignin derivatives. ACS Sustain Chem Eng. 2014;2(5):1106–13.

Xu Z, Qin L, Cai M, et al. Biodegradation of kraft lignin by newly isolated Klebsiella pneumoniae, Pseudomonas putida, and Ochrobactrum tritici strains. Environ Sci Pollut Res. 2018;25:14171.

Yang C, Wang T, Gao L, Yin H, Lu X. Isolation, identification and characterization of lignin-degrading bacteria from Qinling, China. J Appl Microbiol. 2017;123:1447–60.

Akita H, Kimura Z, Yusoff M, et al. Isolation and characterization of Burkholderia sp. strain CCA53 exhibiting ligninolytic potential. SpringerPlus. 2016;5:596.

Jung D, Kim E, Jung E, et al. Production of p-hydroxybenzoic acid from p-coumaric acid by Burkholderia glumae BGR1. Biotechnol Bioeng. 2016;113:1493–503.

Show PL, Tan CP, Anuar MS, et al. Primary recovery of lipase derived from Burkholderia cenocepacia strain ST8 and recycling of phase components in an aqueous two-phase system. Biochem Eng J. 2012;60:74–80.

Adnan M, Li K, Wang J, Xu L, et al. Hierarchical ZIF-8 toward immobilizing Burkholderia cepacia lipase for application in biodiesel preparation. Int J Mol Sci. 2018;19(5):1424.

Kumar H, Dubey RC, Maheshwari DK. Seed-coating fenugreek with Burkholderia rhizobacteria enhances yield in field trials and can combat Fusarium wilt. Rhizosphere. 2017;3:92–9.

Satapute PP, Kaliwal BB. Burkholderia sp. strain BBK_9, a potent agent for propiconazole degradation. In: Bidoia E, Montagnolli R, editors. Toxicity and biodegradation testing. Methods in pharmacology and toxicology. New York: Humana Press; 2018.

Li J, Zhang J, Yadav MP, Li X. Biodegradability and biodegradation pathway of di-(2-ethylhexyl) phthalate by Burkholderia pyrrocinia B1213. Chemosphere. 2019;225:443–50.

Cauduro GP, Falcon T, Leal AL, Valiati VH. Differential expression of genes involved in utilization of benzo(a)pyrene in Burkholderia vietnamiensis G4 strain. In: Mannina G, editor. Frontiers in wastewater treatment and modelling. FICWTM 2017. Lecture Notes in Civil Engineering, vol 4. Cham: Springer.

Thukair AAA, Malik K. Pyrene metabolism by the novel bacterial strains Burkholderia fungorum (T3A13001) and Caulobacter sp. (T2A12002) isolated from an oil-polluted site in the Arabian Gulf. Int Biodeterior Biodegrad. 2016;110:32–7.

Juhasz AL, Britz ML, Stanley GA. Degradation of benzo[a]pyrene, dibenz[a, h]anthracene and coronene by Burkholderia cepacia. Water Sci Technol. 1997;36:45–51.

Kato K, Kozaki S, Sakuranaga M. Degradation of lignin compounds by bacteria from termite guts. Biotechnol Lett. 1998;20:459.

de Gonzalo G, Colpa D, Habib MHM, et al. Bacterial enzymes involved in lignin degradation. J Biotechnol. 2016;236:110–9.

Kumar M, Mishra A, Singh SS, Srivastava S, Thakur IS. Expression and characterization of novel laccase gene from Pandoraea sp. ISTKB and its application. Int J Biol Macromol. 2018;115:308–16.

Kumar M, Singh J, Singh MK, et al. Investigating the degradation process of kraft lignin by β-proteobacterium, Pandoraea sp. ISTKB. Environ Sci Pollut Res. 2015;22:15690.

Chen YH, Chai LY, Zh YH, et al. Biodegradation of Kraft lignin by a bacterial strain Comamonas sp. B-9 isolated from eroded bamboo slips. J Appl Microbiol. 2012;112:900–6.

Bridou R, Monperrus M, Gonzalez PR, et al. Simultaneous determination of mercury methylation and demethylation capacities of various sulfate-reducing bacteria using species-specific isotopic tracers. Environ Toxicol Chem. 2011;30:337–44.

Bernardi M, Tangorra RR, Palmisano P, Bogliano A. Chemicals from renewable sources. Biochemtex—Mossi & Ghisolfi Group. Tortona: Elsevier Inc; 2016.

Kaur B, Chakraborty D, Kumar B. Phenolic biotransformations during conversion of ferulic acid to vanillin by lactic acid bacteria. BioMed Res Int. 2013;2013:590359. https://doi.org/10.1155/2013/590359.

Yan L, Chen P, Zhang S, et al. Biotransformation of ferulic acid to vanillin in the packed bed-stirred fermenters. Sci Rep. 2016;6:34644.

Leewis MC, Uhlik O, Leig MB. Synergistic processing of biphenyl and benzoate: carbon flow through the bacterial community in polychlorinated-biphenyl contaminated soil. Sci Rep. 2016;6:22145.

Tropel D, Meer J. Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev. 2004;68(3):474–500.

Kim Y, Joachimiak G, Bigelow L, Babnigg G, Joachimiak A. How aromatic compounds block dna binding of hcar catabolite regulator. J Biol Chem. 2016;291:13243–56.

Parke D, Ornston LN. Hydroxycinnamate (hca) catabolic genes from Acinetobacter sp. strain ADP1 are repressed by HcaR and are induced by hydroxycinnamoyl coenzyme A thioesters. Appl Environ Microbiol. 2003;69:5398–409.

Kamimura N, Takahashi K, Mori K, et al. Bacterial catabolism of lignin-derived aromatics, new findings in a recent decade, update on bacterial lignin catabolism. Environ Microbiol Rep. 2017;9:679–705.

Kumar M, Verma S, Gazara RK, et al. Genomic and proteomic analysis of lignin degrading and polyhydroxyalkanoate accumulating β-proteobacterium Pandoraea sp. ISTKB. Biotechnol Biofuels. 2018;11:1.

Dukan S, Nystrom T. Oxidative stress defense and deterioration of growth-arrested Escherichia coli cells. J Biol Chem. 1999;274:26027–32.

Seaver LC, Imlay JA. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol. 2001;183(24):7173–81.

Sato Y, Moriuchi H, Hishiyama S, et al. Identification of three alcohol dehydrogenase genes involved in the stereospecific catabolism of arylglycerol-β-aryl ether by Sphingobium sp. strain SYK-6. Appl Environ Microbiol. 2009;75(16):5195–201.

Rashid MM, Zhang X, Wilkinson R, et al. Sphingobacterium sp. T2 manganese superoxide dismutase catalyzes the oxidative demethylation of polymeric lignin via generation of hydroxyl radical. ACS Chem Biol. 2018;13(10):2920–9.

Bugg TD, Ahmad M, Hardiman E, et al. The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol. 2011;22(3):394–400.

Abdelaziz OY, Brink DP, Prothmann J, et al. Biological valorization of low molecular weight lignin. Biotechnol Adv. 2016;34(8):1318–46.

Ma J, Zhang K, Liao H, et al. Genomic and secretomic insight into lignocellulolytic system of an endophytic bacterium Pantoea ananatis Sd-1. Biotechnol Biofuels. 2016;9(1):25.

Thotsaporn K, Tinikul R, Maenpuen S, et al. Enzymes in the p-hydroxyphenylacetate degradation pathway of Acinetobacter baumannii. J Mol Catal B Enzym. 2016;134:353–66.

Deangelis K, Sharma D, Varney R, et al. Evidence supporting dissimilatory and assimilatory lignin degradation in Enterobacter lignolyticus SCF1. Front Microbiol. 2013;4:280.

Zhu D, Zhang P, Xie C, et al. Biodegradation of alkaline lignin by Bacillus ligniniphilus L1. Biotechnol Biofuels. 2017;10(1):44.

Ismail W, Escher J. Epoxy coenzyme A thioester pathways for degradation of aromatic compounds. Appl Environ Microbiol. 2012;78:5043–51.

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

Kumar M, Morya R, Gnansounou E, et al. Characterization of carbon dioxide concentrating chemolithotrophic bacterium Serratia sp. ISTD04 for production of biodiesel. Bioresour Technol. 2017;243:893–7.

Pometto AL 3rd, Sutherland JB, Crawford DL. Streptomyces setonii: catabolism of vanillic acid via guaiacol and catechol. Can J Microbiol. 1981;6:636–8.

Raj K, Krishnan C. High sugar yields from sugarcane (Saccharum officinarum) bagasse using low-temperature aqueous ammonia pretreatment and laccase-mediator assisted enzymatic hydrolysis. Ind Crops Prod. 2018;111:673–83.

Kinnunen AJ, Maijala PM, Jarvinen PP, Hatakka AI. Improved efficiency in screening for lignin-modifying peroxidases and laccases of basidiomycetes. Curr Biotechnol. 2017;6(2):105–15.

Morya R, Kumar M, Thakur IS. Utilization of glycerol by Bacillus sp. ISTVK1 for production and characterization of polyhydroxyvalerate. Bioresour Technol Rep. 2018;2:1–6.

Overbeek R, Olson R, Pusch GD, et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res. 2013;42(D1):D206–14.

Cheong WH, Tan YC, Yap SJ. ClicO FS, an interactive web-based service of Circos. Bioinformatics. 2015;31:3685.

Moriya Y, Itoh M, Okuda S, et al. KAAS, an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:W182–5.

Weber T, Blin K, Duddela S, et al. antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 2015;43(W1):W237–43.

Bertelli C, Laird MR, Williams KP, et al. IslandViewer 4, expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res. 2017;45:30–5.

Janusz G, Pawlik A, Sulej J, Swiderska-Burek U, Jarosz-Wilkolazka A, Paszczynski A. Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol Rev. 2017;41(6):941–62.

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Biotechnology for Biofuels

Tập 12 Số 1

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