Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria
Language English Country United States Media electronic-ecollection
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
24551229
PubMed Central
PMC3923840
DOI
10.1371/journal.pone.0089108
PII: PONE-D-13-49157
Knihovny.cz E-resources
- MeSH
- Bacterial Proteins biosynthesis MeSH
- beta-Glucosidase biosynthesis MeSH
- Biodegradation, Environmental MeSH
- Biomass MeSH
- Cellulose 1,4-beta-Cellobiosidase biosynthesis MeSH
- Cellulose metabolism MeSH
- Hydrolysis MeSH
- Catechols metabolism MeSH
- Kinetics MeSH
- Lignin metabolism MeSH
- Populus chemistry MeSH
- Soil Microbiology * MeSH
- Carbon Radioisotopes MeSH
- Streptomyces enzymology isolation & purification MeSH
- Trees chemistry MeSH
- Xylosidases biosynthesis MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Bacterial Proteins MeSH
- beta-Glucosidase MeSH
- catechol MeSH Browser
- Cellulose 1,4-beta-Cellobiosidase MeSH
- Cellulose MeSH
- exo-1,4-beta-D-xylosidase MeSH Browser
- Catechols MeSH
- Lignin MeSH
- Carbon Radioisotopes MeSH
- Xylosidases MeSH
While it is known that several Actinobacteria produce enzymes that decompose polysaccharides or phenolic compounds in dead plant biomass, the occurrence of these traits in the environment remains largely unclear. The aim of this work was to screen isolated actinobacterial strains to explore their ability to produce extracellular enzymes that participate in the degradation of polysaccharides and their ability to cometabolically transform phenolic compounds of various complexities. Actinobacterial strains were isolated from meadow and forest soils and screened for their ability to grow on lignocellulose. The potential to transform (14)C-labelled phenolic substrates (dehydrogenation polymer (DHP), lignin and catechol) and to produce a range of extracellular, hydrolytic enzymes was investigated in three strains of Streptomyces spp. that possessed high lignocellulose degrading activity. Isolated strains showed high variation in their ability to produce cellulose- and hemicellulose-degrading enzymes and were able to mineralise up to 1.1% and to solubilise up to 4% of poplar lignin and to mineralise up to 11.4% and to solubilise up to 64% of catechol, while only minimal mineralisation of DHP was observed. The results confirm the potential importance of Actinobacteria in lignocellulose degradation, although it is likely that the decomposition of biopolymers is limited to strains that represent only a minor portion of the entire community, while the range of simple, carbon-containing compounds that serve as sources for actinobacterial growth is relatively wide.
See more in PubMed
Baldrian P, Šnajdr J (2011) Lignocellulose-Degrading Enzymes in Soils. In: Shukla G, Varma A, editors. Soil Enzymology. Berlin: Springer-Verlag Berlin. p.167–186.
de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795–811. PubMed
Baldrian P (2008) Enzymes of Saprotrophic Basidiomycetes. In: Boddy L, Frankland JC, VanWest P, editors. Ecology of Saprotrophic Basidiomycetes. San Diego: Elsevier Academic Press Inc. p.19–41.
Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, et al. (2011) The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi. Science 333: 762–765. PubMed
Floudas D, Binder M, Riley R, Barry K, Blanchette RA, et al. (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336: 1715–1719. PubMed
Sjöström E (1993) Wood chemistry: Fundamentals and applications. 2nd edition ed: Academic Press (San Diego).
Martinez AT, Speranza M, Ruiz-Duenas FJ, Ferreira P, Camarero S, et al. (2005) Biodegradation of lignocellulosics: microbial chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8: 195–204. PubMed
Theuerl S, Buscot F (2010) Laccases: toward disentangling their diversity and functions in relation to soil organic matter cycling. Biol Fertil Soils 46: 215–225.
Baldrian P, Voříšková J, Dobiášová P, Merhautová V, Lisá L, et al. (2011) Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338: 111–125.
Berlemont R, Martiny AC (2013) Phylogenetic Distribution of Potential Cellulases in Bacteria. Appl Environ Microbiol 79: 1545–1554. PubMed PMC
Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol Mol Biol Rev 66: 506–577. PubMed PMC
Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80: 735–746. PubMed
Chater KF, Biro S, Lee KJ, Palmer T, Schrempf H (2010) The complex extracellular biology of Streptomyces . FEMS Microbiol Rev 34: 171–198. PubMed
Warren RAJ (1996) Microbial hydrolysis of polysaccharides. Annu Rev Microbiol 50: 183–212. PubMed
McCarthy AJ (1987) Lignocellulose-degrading actinomycetes. FEMS Microbiol Rev 46: 145–163.
Enkhbaatar B, Temuujin U, Lim JH, Chi WJ, Chang YK, et al. (2012) Identification and Characterization of a Xyloglucan-Specific Family 74 Glycosyl Hydrolase from Streptomyces coelicolor A3(2). Appl Environ Microbiol 78: 607–611. PubMed PMC
Sun Y, Cheng JJ, Himmel ME, Skory CD, Adney WS, et al. (2007) Expression and characterization of Acidothermus cellulolyticus E1 endoglucanase in transgenic duckweed Lemna minor 8627. Biores Technol 98: 2866–2872. PubMed
Yin LJ, Huang PS, Lin HH (2010) Isolation of Cellulase-Producing Bacteria and Characterization of the Cellulase from the Isolated Bacterium Cellulomonas Sp YJ5. J Agric Food Chem 58: 9833–9837. PubMed
Song JM, Wei DZ (2010) Production and characterization of cellulases and xylanases of Cellulosimicrobium cellulans grown in pretreated and extracted bagasse and minimal nutrient medium M9. Biomass Bioenergy 34: 1930–1934.
Yoon MH, Choi WY (2007) Characterization and action patterns of two beta-1,4-glucanases purified from Cellulomonas uda CS1–1. J Microbiol Biotechnol 17: 1291–1299. PubMed
Zhang F, Hu SN, Chen JJ, Lin LB, Wei YL, et al. (2012) Purification and partial characterisation of a thermostable xylanase from salt-tolerant Thermobifida halotolerans YIM 90462(T). Process Biochem 47: 225–228.
An DS, Cui CH, Lee HG, Wang L, Kim SC, et al. (2010) Identification and Characterization of a Novel Terrabacter ginsenosidimutans sp nov beta-Glucosidase That Transforms Ginsenoside Rb1 into the Rare Gypenosides XVII and LXXV. Appl Environ Microbiol 76: 5827–5836. PubMed PMC
Fan HX, Miao LL, Liu Y, Liu HC, Liu ZP (2011) Gene cloning and characterization of a cold-adapted beta-glucosidase belonging to glycosyl hydrolase family 1 from a psychrotolerant bacterium Micrococcus antarcticus . Enzyme Microb Technol 49: 94–99. PubMed
Nakano H, Okamoto K, Yatake T, Kiso T, Kitahata S (1998) Purification and characterization of a novel beta-glucosidase from Clavibacter michiganense that hydrolyzes glucosyl ester linkage in steviol glycosides. J Ferment Bioeng 85: 162–168.
Nunoura N, Ohdan K, Yano T, Yamamoto K, Kumagai H (1996) Purification and characterization of beta-D-glucosidase (beta-D-fucosidase) from Bifidobacterium breve clb acclimated to cellobiose. Biosci Biotechnol Biochem 60: 188–193. PubMed
Quan LH, Min JW, Jin Y, Wang C, Kim YJ, et al. (2012) Enzymatic Biotransformation of Ginsenoside Rb1 to Compound K by Recombinant beta-Glucosidase from Microbacterium esteraromaticum . J Agric Food Chem 60: 3776–3781. PubMed
Anderson I, Abt B, Lykidis A, Klenk HP, Kyrpides N, et al. (2012) Genomics of Aerobic Cellulose Utilization Systems in Actinobacteria . PLOS One 7: e39331. PubMed PMC
Khanna S (1993) Gauri (1993) Regulation, purification, and properties of xylanase from Cellulomonas fimi . Enzyme Microb Technol 15: 990–995.
Li CJ, Hong YZ, Shao ZZ, Lin L, Huang XL, et al. (2009) Novel Alkali-Stable, Cellulase-Free Xylanase from Deep-Sea Kocuria sp Mn22. J Microbiol Biotechnol 19: 873–880. PubMed
Oh HW, Heo SY, Kim DY, Park DS, Bae KS, et al. (2008) Biochemical characterization and sequence analysis of a xylanase produced by an exo-symbiotic bacterium of Gryllotalpa orientalis, Cellulosimicrobium sp HY-12. Ant Leeuw Int J Gen Mol Microbiol 93: 437–442. PubMed
Petrosyan P, Luz-Madrigal A, Huitrón C, Flores M (2002) Characterization of a xylanolytic complex from Streptomyces sp. Biotechnol Lett 24: 1473–1476.
Robinson LE, Crawford RL (1978) Degradation of 14C-labelled lignins by Bacillus megaterium . FEMS Microbiol Lett 4: 301–302.
Vicuna R (1988) Bacterial degradation of lignin. Enzyme Microb Technol 10: 646–655.
Zimmermann W (1990) Degradation of lignin by bacteria. J Biotechnol 13: 119–130.
Cartwrig N, Holdom KS (1973) Enzymic lignin, its release and utilization by bacteria. Microbios 8: 7–14. PubMed
Crawford DL, Barder MJ, Pometto AL, Crawford RL (1982) Chemistry of softwood lignin degradation by Streptomyces viridosporus . Arch Microbiol 131: 140–145.
Sutherland JB, Blanchette RA, Crawford DL, Pometto AL (1979) Breakdown of Douglas fir phloem by a lignocellulose-degrading Streptomyces . Curr Microbiol 2: 123–126.
Trojanowski J, Haider K, Sundman V (1977) Decomposition of 14C-labelled lignin and phenols by a Nocardia sp. Arch Microbiol 114: 149–153. PubMed
Caliz J, Montserrat G, Marti E, Sierra J, Chung AP, et al. (2013) Emerging resistant microbiota from an acidic soil exposed to toxicity of Cr, Cd and Pb is mainly influenced by the bioavailability of these metals. J Soils Sediments 13: 413–428.
Harichova J, Karelova E, Pangallo D, Ferianc P (2012) Structure analysis of bacterial community and their heavy-metal resistance determinants in the heavy-metal-contaminated soil sample. Biologia 67: 1038–1048.
Mühlbachová G (2011) Soil microbial activities and heavy metal mobility in long-term contaminated soils after addition of EDTA and EDDS. Ecol Eng 37: 1064–1071.
Hayakawa M, Nonomura H (1987) Humic acid-vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65: 501–509.
Hayakawa M, Momose Y, Yamazaki T, Nonomura H (1996) A method for the selective isolation of Microtetraspora glauca and related four-spored actinomycetes from soil. J Appl Bacteriol 80: 375–386.
Baldrian P (2009) Microbial enzyme-catalyzed processes in soils and their analysis. Plant Soil Environ 55: 370–378.
Valášková V, Šnajdr J, Bittner B, Cajthaml T, Merhautová V, et al. (2007) Production of lignocellulose-degrading enzymes and degradation of leaf litter by saprotrophic basidiomycetes isolated from a Quercus petraea forest. Soil Biol Biochem 39: 2651–2660.
Brunow G, Ammalahti E, Niemi T, Sipila J, Simola LK, et al. (1998) Labelling of a lignin from suspension cultures of Picea abies . Phytochem 47: 1495–1500.
Tuomela M, Oivanen P, Hatakka A (2002) Degradation of synthetic 14C-lignin by various white-rot fungi in soil. Soil Biol Biochem 34: 1613–1620.
Odier E, Janin G, Monties B (1981) Poplar Lignin Decomposition by Gram-Negative Aerobic Bacteria. Appl Environ Microbiol 41: 337–341. PubMed PMC
Šnajdr J, Steffen KT, Hofrichter M, Baldrian P (2010) Transformation of 14C-labelled lignin and humic substances in forest soil by the saprobic basidiomycetes Gymnopus erythropus and Hypholoma fasciculare . Soil Biol Biochem 42: 1541–1548.
Sagova-Mareckova M, Cermak L, Novotna J, Plhackova K, Forstova J, et al. (2008) Innovative methods for soil DNA purification tested in soils with widely differing characteristics. Appl Environ Microbiol 74: 2902–2907. PubMed PMC
Šnajdr J, Cajthaml T, Valášková V, Merhautová V, Petránková M, et al. (2011) Transformation of Quercus petraea litter: successive changes in litter chemistry are reflected in differential enzyme activity and changes in the microbial community composition. FEMS Microbiol Ecol 75: 291–303. PubMed
She YL, Li XT, Sun BG, Lv YG, Song HX (2012) Screening of Actinomycetes with High Producing Xylanase. Adv Mat Res 365: 332–337.
Wang G, Meng K, Luo H, Wang Y, Huang H, et al. (2012) Phylogenetic Diversity and Environment-Specific Distributions of Glycosyl Hydrolase Family 10 Xylanases in Geographically Distant Soils. PLOS One 7: e43480. PubMed PMC
Post DA, Luebke VE (2005) Purification, cloning, and properties of beta-galactosidase from Saccharopolyspora erythraea and its use as a reporter system. Appl Microbiol Biotechnol 67: 91–96. PubMed
Shi P, Yao G, Cao Y, Yang P, Yuan T, et al. (2011) Cloning and characterization of a new β-mannosidase from Streptomyces sp. S27. Enzyme Microb Technol 49: 277–283. PubMed
Tajana E, Fiechter A, Zimmermann W (1992) Purification and characerization of two alpha-L-arabinofuranosidases from Streptomyces diastaticus . Appl Environ Microbiol 58: 1447–1450. PubMed PMC
Crawford DL (1978) Lignocellulose decomposition by selected streptomyces strains. Appl Environ Microbiol 35: 1041–1045. PubMed PMC
Pasti MB, Pometto AL, Nuti MP, Crawford DL. Lignin-solubilizing ability of actinomycetes isolated from termite (Termitidae) gut. Appl Environ Microbiol 56: 2213–2218. PubMed PMC
Kerr TJ, Kerr RD, Benner R (1983) Isolation of a Bacterium Capable of Degrading Peanut Hull Lignin. Appl Environ Microbiol 46: 1201–1206. PubMed PMC
Krastanov A, Alexieva Z, Yemendzhiev H (2013) Microbial degradation of phenol and phenolic derivatives. Eng Life Sci 13: 76–87.
El Azhari N, Devers-Lamrani M, Chatagnier G, Rouard N, Martin-Laurent F (2010) Molecular analysis of the catechol-degrading bacterial community in a coal wasteland heavily contaminated with PAHs. J Hazard Mater 177: 593–601. PubMed
Osono T, Takeda H (2005) Decomposition of organic chemical components in relation to nitrogen dynamics in leaf litter of 14 tree species in a cool temperate forest. Ecol Res 20: 41–49.
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