Abstract
Lignocellulosic biomasses, either from non-edible plants or from agricultural residues, stock biomacromolecules that can be processed to produce both energy and bioproducts. Therefore, they become major candidates to replace petroleum as the main source of energy. However, to shift the fossil-based economy to a bio-based one, it is imperative to develop robust biotechnologies to efficiently convert lignocellulosic streams in power and platform chemicals. Although most of the biomass processing facilities use celluloses and hemicelluloses to produce bioethanol and paper, there is no consolidated bioprocess to produce valuable compounds out of lignin at industrial scale available currently. Usually, lignin is burned to provide heat or it remains as a by-product in different streams, thus arising environmental concerns. In this way, the biorefinery concept is not extended to completion. Due to Nature offers an arsenal of biotechnological tools through microorganisms to accomplish lignin valorization or degradation, an increasing number of projects dealing with these tasks have been described recently. In this review, outstanding reports over the last 6 years are described, comprising the microbial utilization of lignin to produce a variety of valuable compounds as well as to diminish its ecological impact. Furthermore, perspectives on these topics are given.
Similar content being viewed by others
References
Ahmad M, Taylor CR, Pink D, Burton K, Eastwood D, Bending GD, Bugg TD (2010) Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders. Mol BioSyst 6:815–821. doi:10.1039/b908966g
Akita H, Kimura Z-I, Yusoff MZM, Nakashima N, Hoshino T (2016) Isolation and characterization of Burkholderia sp. strain CCA53 exhibiting ligninolytic potential. Springerplus 5:596. doi:10.1186/s40064-016-2237-y
Arantes V, Jellison J, Goodell B (2012) Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass. Appl Microbiol Biotechnol 94:323–338. doi:10.1007/s00253-012-3954-y
Arimoto M et al (2015) Molecular breeding of lignin-degrading brown-rot fungus Gloeophyllum trabeum by homologous expression of laccase gene. AMB Express 5:81. doi:10.1186/s13568-015-0173-9
Armstrong Z, Mewis K, Strachan C, Hallam SJ (2015) Biocatalysts for biomass deconstruction from environmental genomics. Curr Opin Chem Biol 29:18–25. doi:10.1016/j.cbpa.2015.06.032
Arun A, Eyini M (2011) Comparative studies on lignin and polycyclic aromatic hydrocarbons degradation by basidiomycetes fungi. Bioresour Technol 102:8063–8070. doi:10.1016/j.biortech.2011.05.077
Bandounas L, Wierckx NJ, de Winde JH, Ruijssenaars HJ (2011) Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential. BMC Biotechnol 11:94. doi:10.1186/1472-6750-11-94
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
Brown ME, Chang MC (2014) Exploring bacterial lignin degradation. Curr Opin Chem Biol 19:1–7. doi:10.1016/j.cbpa.2013.11.015
Bugg TD, Ahmad M, Hardiman EM, Rahmanpour R (2011a) Pathways for degradation of lignin in bacteria and fungi. Nat Product Rep 28:1883–1896. doi:10.1039/c1np00042j
Bugg TD, Ahmad M, Hardiman EM, Singh R (2011b) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400. doi:10.1016/j.copbio.2010.10.009
Chang AJ, Fan J, Wen X (2012) Screening of fungi capable of highly selective degradation of lignin in rice straw. Int Biodeterior Biodegradation 72:26–30. doi:10.1016/j.ibiod.2012.04.013
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. doi:10.1111/j.1365-2672.2012.05275.x
Cragg SM et al (2015) Lignocellulose degradation mechanisms across the tree of life. Curr Opin Chem Biol 29:108–119. doi:10.1016/j.cbpa.2015.10.018
Curran KA, Leavitt JM, Karim AS, Alper HS (2013) Metabolic engineering of muconic acid production in Saccharomyces cerevisiae. Metab Eng 15:55–66. doi:10.1016/j.ymben.2012.10.003
Dashtban M, Schraft H, Syed TA, Qin W (2010) Fungal biodegradation and enzymatic modification of lignin. Int J Biochem Mol Biol 1:36–50
Davis JR, Sello JK (2010) Regulation of genes in Streptomyces bacteria required for catabolism of lignin-derived aromatic compounds. Appl Microbiol Biotechnol 86:921–929. doi:10.1007/s00253-009-2358-0
DeMartini JD, Pattathil S, Miller JS, Li H, Hahn MG, Wyman CE (2013) Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass. Energy Environ Sci 6:898–909. doi:10.1039/C3EE23801F
Elsalam HE, Bahobail AS (2016) Lignin biodegradation by thermophilic bacterial isolates from Saudi Arabia research journal of pharmaceutical. Biol Chem Sci 7:1413–1424
Eudes A, Liang Y, Mitra P, Loqué D (2014) Lignin bioengineering. Curr Opin Biotechnol 26:189–198. doi:10.1016/j.copbio.2014.01.002
Fache M, Darroman E, Besse V, Auvergne R, Caillol S, Boutevin B (2014) Vanillin, a promising biobased building-block for monomer synthesis. Green Chem 16:1987–1998. doi:10.1039/C3GC42613K
Fang W et al (2012) Evidence for lignin oxidation by the giant panda fecal microbiome. PLoS ONE 7:e50312. doi:10.1371/journal.pone.0050312
Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol 9:803–816. doi:10.1038/nrmicro2652
Gilbert JA, Jansson JK, Knight R (2014) The Earth Microbiome project: successes and aspirations. BMC Biol 12:1–4. doi:10.1186/s12915-014-0069-1
Hainal A, Capraru A, Volf I, Popa V (2012) Lignin as a carbon source for the cultivation of some Rhodotorula species. Cellul Chem Technol 46:87–96
Harith Z, Ibrahim NA, Yusoff N (2014) Isolation and identification of locally isolated lignin degrading bacteria. J Sustain Sci Manag 9:114–118
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
Johnson CW, Salvachúa D, Khanna P, Smith H, Peterson DJ, Beckham GT (2016) Enhancing muconic acid production from glucose and lignin-derived aromatic compounds via increased protocatechuate decarboxylase activity. Metab Eng Commun 3:111–119. doi:10.1016/j.meteno.2016.04.002
Kameshwar AK, Qin W (2016) Recent developments in using advanced sequencing technologies for the genomic studies of lignin and cellulose degrading microorganisms. Int J Biol Sci 12:156–171. doi:10.7150/ijbs.13537
Kawaguchi H, Hasunuma T, Ogino C, Kondo A (2016) Bioprocessing of bio-based chemicals produced from lignocellulosic feedstocks. Curr Opin Biotechnol 42:30–39. doi:10.1016/j.copbio.2016.02.031
Knežević A, Stajić M, Jovanović VM, Kovačević V, Ćilerdžić J, Milovanović I, Vukojević J (2016) Induction of wheat straw delignification by Trametes species Scientific Reports 6:26529 doi:10.1038/srep26529 http://www.nature.com/articles/srep26529#supplementary-information
Korniłłowicz-Kowalska T, Rybczyńska K (2015) Screening of microscopic fungi and their enzyme activities for decolorization and biotransformation of some aromatic compounds. Int J Environ Sci Technol 12:2673–2686. doi:10.1007/s13762-014-0656-2
Kosa M, Ragauskas AJ (2012) Bioconversion of lignin model compounds with oleaginous Rhodococci. Appl Microbiol Biotechnol 93:891–900. doi:10.1007/s00253-011-3743-z
Kosa M, Ragauskas AJ (2013) Lignin to lipid bioconversion by oleaginous Rhodococci. Green Chem 15:2070–2074. doi:10.1039/C3GC40434J
Kulikova HA, Kliain OI, Stepanova EV, Koroleva OV (2011) Use of basidiomycetes in industrial waste processing and utilization technologies: fundamental and applied aspects (review). Prikl Biokhim Mikrobiol 47:619–634
Li C, Zhao X, Wang A, Huber GW, Zhang T (2015) Catalytic transformation of lignin for the production of chemicals and fuels. Chem Rev 115:11559–11624. doi:10.1021/acs.chemrev.5b00155
Liang YS et al (2010) Biodelignification of rice straw by Phanerochaete chrysosporium in the presence of dirhamnolipid. Biodegradation 21:615–624. doi:10.1007/s10532-010-9329-0
Lomascolo A, Uzan-Boukhris E, Herpoel-Gimbert I, Sigoillot JC, Lesage-Meessen L (2011) Peculiarities of Pycnoporus species for applications in biotechnology. Appl Microbiol Biotechnol 92:1129–1149. doi:10.1007/s00253-011-3596-5
Lv Y, Chen Y, Sun S, Hu Y (2014) Interaction among multiple microorganisms and effects of nitrogen and carbon supplementations on lignin degradation. Bioresour Technol 155:144–151. doi:10.1016/j.biortech.2013.12.012
Maity SK (2015) Opportunities, recent trends and challenges of integrated biorefinery: part II. Renew Sustain Energy Rev 43:1446–1466. doi:10.1016/j.rser.2014.08.075
Makela MR, Donofrio N, de Vries RP (2014) Plant biomass degradation by fungi. Fungal Genet Biol 72:2–9. doi:10.1016/j.fgb.2014.08.010
Mathews SL, Grunden AM, Pawlak J (2016) Degradation of lignocellulose and lignin by Paenibacillus glucanolyticus. Int Biodeterior Biodegradation 110:79–86. doi:10.1016/j.ibiod.2016.02.012
McCann MC, Carpita NC (2015) Biomass recalcitrance: a multi-scale, multi-factor, and conversion-specific property. J Exp Bot 66:4109–4118. doi:10.1093/jxb/erv267
McLeod MP et al (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103:15582–15587. doi:10.1073/pnas.0607048103
Mottiar Y, Vanholme R, Boerjan W, Ralph J, Mansfield SD (2016) Designer lignins: harnessing the plasticity of lignification. Curr Opin Biotechnol 37:190–200. doi:10.1016/j.copbio.2015.10.009
Mycroft Z, Gomis M, Mines P, Law P, Bugg TDH (2015) Biocatalytic conversion of lignin to aromatic dicarboxylic acids in Rhodococcus jostii RHA1 by re-routing aromatic degradation pathways. Green Chem 17:4974–4979. doi:10.1039/C5GC01347J
Palazzolo MA, Mascotti ML, Lewkowicz ES, Kurina-Sanz M (2015) Self-sufficient redox biotransformation of lignin-related benzoic acids with Aspergillus flavus. J Ind Microbiol Biotechnol 42:1581–1589. doi:10.1007/s10295-015-1696-4
Paliwal R, Rawat AP, Rawat M, Rai JP (2012) Bioligninolysis: recent updates for biotechnological solution. Appl Biochem Biotechnol 167:1865–1889. doi:10.1007/s12010-012-9735-3
Paliwal R, Uniyal S, Rai JP (2015) Evaluating the potential of immobilized bacterial consortium for black liquor biodegradation. Environ Sci Pollut Res Int 22:6842–6853. doi:10.1007/s11356-014-3872-x
Ryazanova TV, Chuprova NA, Luneva TA (2015) Effect of trichoderma fungi on lignin from tree species barks. Catal Ind 7:82–89. doi:10.1134/s2070050415010134
Sainsbury PD, Hardiman EM, Ahmad M, Otani H, Seghezzi N, Eltis LD, Bugg TDH (2013) Breaking down lignin to high-value chemicals: the conversion of lignocellulose to vanillin in a gene deletion mutant of Rhodococcus jostii RHA1. ACS Chem Biol 8:2151–2156. doi:10.1021/cb400505a
Salvachua D, Karp EM, Nimlos CT, Vardon DR, Beckham GT (2015) Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria. Green Chem 17:4951–4967. doi:10.1039/C5GC01165E
Sharma RK, Arora DS (2015) Fungal degradation of lignocellulosic residues: an aspect of improved nutritive quality. Crit Rev Microbiol 41:52–60. doi:10.3109/1040841x.2013.791247
Sonoki T, Morooka M, Sakamoto K, Otsuka Y, Nakamura M, Jellison J, Goodell B (2014) Enhancement of protocatechuate decarboxylase activity for the effective production of muconate from lignin-related aromatic compounds. J Biotechnol 192(Pt A):71–77. doi:10.1016/j.jbiotec.2014.10.027
Strachan CR et al (2014) Metagenomic scaffolds enable combinatorial lignin transformation. Proc Natl Acad Sci USA 111:10143–10148. doi:10.1073/pnas.1401631111
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
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 113:521–530. doi:10.1111/j.1365-2672.2012.05352.x
Tian JH, Pourcher AM, Bouchez T, Gelhaye E, Peu P (2014) Occurrence of lignin degradation genotypes and phenotypes among prokaryotes. Appl Microbiol Biotechnol 98:9527–9544. doi:10.1007/s00253-014-6142-4
Upton BM, Kasko AM (2016) Strategies for the conversion of lignin to high-value polymeric materials: review and perspective. Chem Rev 116:2275–2306. doi:10.1021/acs.chemrev.5b00345
van Kuijk SJ, Sonnenberg AS, Baars JJ, Hendriks WH, Cone JW (2015) Fungal treated lignocellulosic biomass as ruminant feed ingredient: a review. Biotechnol Adv 33:191–202. doi:10.1016/j.biotechadv.2014.10.014
Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905. doi:10.1104/pp.110.155119
Wang Y, Liu Q, Yan L, Gao Y, Wang Y, Wang W (2013) A novel lignin degradation bacterial consortium for efficient pulping. Bioresour Technol 139:113–119. doi:10.1016/j.biortech.2013.04.033
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 17:2784–2789. doi:10.1039/C5GC00422E
Yang YS, Zhou JT, Lu H, Yuan YL, Zhao LH (2012) Isolation and characterization of Streptomyces spp. strains F-6 and F-7 capable of decomposing alkali lignin. Environ Technol 33:2603–2609. doi:10.1080/09593330.2012.672473
Yue ZB, Li WW, Yu HQ (2013) Application of rumen microorganisms for anaerobic bioconversion of lignocellulosic biomass. Bioresour Technol 128:738–744. doi:10.1016/j.biortech.2012.11.073
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 27:38–45. doi:10.1016/j.copbio.2013.09.008
Zhao C, Xie S, Pu Y, Zhang R, Huang F, Ragauskas AJ, Yuan JS (2016) Synergistic enzymatic and microbial lignin conversion. Green Chem 18:1306–1312. doi:10.1039/C5GC01955A
Zheng Y, Chai LY, Yang ZH, Tang CJ, Chen YH, Shi Y (2013) Enhanced remediation of black liquor by activated sludge bioaugmented with a novel exogenous microorganism culture. Appl Microbiol Biotechnol 97:6525–6535. doi:10.1007/s00253-012-4453-x
Acknowledgments
This work was supported by Grants from Universidad Nacional de San Luis PROICO 2-1716, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) PIP 1122015 0100090 and PDTS 2014-094, and Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) PICT 2014-0654. MAP is a postdoctoral CONICET fellow and MKS is member of the Research Career of CONICET, Argentina.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no commercial or financial conflict of interest.
Rights and permissions
About this article
Cite this article
Palazzolo, M.A., Kurina-Sanz, M. Microbial utilization of lignin: available biotechnologies for its degradation and valorization. World J Microbiol Biotechnol 32, 173 (2016). https://doi.org/10.1007/s11274-016-2128-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-016-2128-y