Lignocellulose-degrading actinomycetes

Abstract Increasing interest in the exploitation of plant biomass as a renewable resource has provided an impetus for research on microbial degradation of lignocellulose. This has traditionally been concentrated on the fungi, but lignocellulose-degrading prokaryotes are beginning to receive more attention. Strain improvement by genetic manipulation, and large-scale cultivation are more easily achieved in prokaryotes, and the actinomycetes are no exception. In addition, their growth as branching hyphae is well adapted to the penetration and degradation of insoluble substrates such as lignocellulose. Actinomycetes form an important part of the microbial community responsible for nutrient recycling in natural substrates. Their specific contribution to lignocellulose degradation in the environment has received only limited attention but their importance can be inferred from the ubiquity and diversity of species in which activity against lignocellulose has been demonstrated. Characterisation of the cellulolytic activity of actinomycetes has understandably received most attention, since cellulose is the major component of plant biomass and a potentially utilisable source of glucose. Actinomycete cellulases are inducible extracellular enzymes which appear to attack cellulose in much the same way as fungal hydrolytic cellulases. Actinomycete xylanases similarly conform to the basic patterns of production and activity established in other bacteria and fungi, but they have been relatively little-studied. Evidence for activity against lignin has only recently been obtained for actinomycetes, with the development of sensitive radiometric assays which permit detection of limited ligninolytic activity. There is little doubt that actinomycetes compare poorly with the whiterot fungi in relation to the extent of delignification achieved, particularly with wood lignocelluloses. Nevertheless, their ability to solubilise grass lignins may have a role in humification and biotechnological applications of lignocellulose conversion. The biochemistry of lignin degradation by actinomycetes remains poorly understood and the enzymes involved have yet to be identified. There is more information on the enzymology of cellulose and hemicellulose degradation, but how these different groups of enzymes and their component proteins interact to solubilise lignocellulose is largely unknown. Elucidation of the biochemistry of lignocellulose degradation and development of actinomycete-based systems for lignocellulose conversion should be greatly assisted by the application of the recombinant DNA techniques recently developed for this group of organisms.

[1]  J. Zeikus,et al.  Preparation and microbial decomposition of synthetic [14C]ligins. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[2]  R. Crawford,et al.  Recent advances in studies of the mechanisms of microbial degradation of lignins , 1984 .

[3]  D. Johnston,et al.  The occurrence and distribution of actinomycetes in lakes of the English Lake District , 1976 .

[4]  M. Okanishi,et al.  Molecular cloning of a xylanase gene from Streptomyces sp. No. 36a and its expression in streptomycetes. , 1986, The Journal of antibiotics.

[5]  James P. Martin,et al.  Decomposition in Soil of 14C-labeled Coumaryl Alcohols; Free and Linked into Dehydropolymer and Plant Lignins and Model Humic Acids , 1977 .

[6]  T. Rowbotham,et al.  Ecology of Rhodococcus coprophilus and Associated Actinomycetes in Fresh Water and Agricultural Habitats , 1977 .

[7]  E. Pye,et al.  Effect of cellobiose, glucose, ethanol, and metal ions on the cellulase enzyme complex of Thermomonospora fusca , 1983, Biotechnology and bioengineering.

[8]  D. Robert,et al.  Carbon-13 NMR Spectra of Lignins, 8. Structural Differences between Lignins of Hardwoods, Softwoods, Grasses and Compression Wood , 1981 .

[9]  D. Crawford,et al.  Catabolic Fate of Streptomyces viridosporus T7A-Produced, Acid-Precipitable Polymeric Lignin upon Incubation with Ligninolytic Streptomyces Species and Phanerochaete chrysosporium , 1986, Applied and environmental microbiology.

[10]  J. Azuma,et al.  Lignin-Carbohydrate Complexes and Phenolic Acids in Bagasse , 1984 .

[11]  J. Dutkiewicz,et al.  Isolation of Actinomycetes and fungi from mouldy hay using a sedimentation chamber. , 1976, The Journal of applied bacteriology.

[12]  R. H. Baltz,et al.  Cloning and Expression in Streptomyces lividans of Clustered Erythromycin Biosynthesis Genes from Streptomyces erythreus , 1986, Bio/Technology.

[13]  G. L. Miller Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar , 1959 .

[14]  T. Kirk,et al.  Formation and action of the ligninolytic system in Basidiomycetes , 1982 .

[15]  E. Pye,et al.  Effect of glucose and other sugars on the β‐1,4‐glucosidase activity of Thermomonospora fusca , 1983, Biotechnology and bioengineering.

[16]  R. Crawford,et al.  Lignin Degradation by Streptomyces viridosporus: Isolation and Characterization of a New Polymeric Lignin Degradation Intermediate , 1983, Applied and environmental microbiology.

[17]  J. Kenten,et al.  Cloning and expression of an extracellular α-amylase gene from Streptomyces hygroscopicus in Streptomyces lividans 66 , 1986 .

[18]  T. Wood,et al.  The cellulase of Trichoderma koningii. Purification and properties of some endoglucanase components with special reference to their action on cellulose when acting alone and in synergism with the cellobiohydrolase. , 1978, The Biochemical journal.

[19]  E. Pye,et al.  Cellulolytic Enzyme System of Thermoactinomyces sp. Grown on Microcrystalline Cellulose , 1978, Applied and environmental microbiology.

[20]  F. Stutzenberger Cellulolytic activity of Thermomonospora curvata: nutritional requirments for cellulase production. , 1972, Applied microbiology.

[21]  M. Pasti,et al.  Cellulolytic activity of Actinomycetes isolated from termites (Termitidae) gut , 1985 .

[22]  M. F. Oberbacher,et al.  Response of Oxidation and Phosphorylation in Citrus Mitochondria to Arsenate , 1965, Nature.

[23]  R. Crawford,et al.  Microbial Degradation of Lignocellulose: the Lignin Component , 1976, Applied and environmental microbiology.

[24]  M. D. Enger,et al.  Multiple Cellulase System from Streptomyces antibioticus , 1965, Journal of bacteriology.

[25]  F. Rombouts,et al.  The cellulase of Trichoderma viride , 1985 .

[26]  D. Crawford Microbial conversions of lignin to useful chemicals using a lignin-degrading Streptomyces , 1981 .

[27]  H. Lechevalier,et al.  Chemical composition as a criterion in the classification of aerobic actinomycetes , 1970 .

[28]  E. Pye,et al.  Saccharification of cellulose by the cellulolytic enzyme system of Thermomonospora sp. II. Hydrolysis of cellulosic substrates , 1980 .

[29]  D. Kluepfel,et al.  Characterization of cellulase and xylanase activities of Streptomyces lividans , 1986, Applied Microbiology and Biotechnology.

[30]  D. Johnston,et al.  Actinomycetes in lake muds: dormant spores or metabolically active mycelium? , 1976 .

[31]  D. Irwin,et al.  Purification and characterization of two β-1,4-endoglucanases from Thermomonospora fusca , 1985 .

[32]  C. MacKenzie,et al.  Streptomyces flavogriseus cellulase: Evaluation under various hydrolysis conditions , 1984, Biotechnology and bioengineering.

[33]  D. Kluepfel,et al.  Cellulase complex of a mesophilic Streptomyces strain. , 1980, Canadian journal of microbiology.

[34]  G. Williams PERICHOLANGIOLITIC BILIARY CIRRHOSIS. , 1965, The Journal of pathology and bacteriology.

[35]  H. Meyer,et al.  Cellulase production by wild and a new mutant strain of Thermomonospora sp. , 1982, Biotechnology and bioengineering.

[36]  W. D. Bellamy Single cell proteins from cellulosic wastes , 1974 .

[37]  F. Stutzenberger,et al.  Cyclic AMP levels during induction and repression of cellulase biosynthesis in Thermomonospora curvata , 1984, Journal of bacteriology.

[38]  D. Kluepfel,et al.  Comparison of β-Glucosidase Activities in Different Streptomyces Strains , 1983 .

[39]  R. E. Hungate Studies on Cellulose Fermentation , 1946, Journal of bacteriology.

[40]  D. Crawford,et al.  Production of microbial protein from waste cellulose by Thermomonospora fusca, a thermophilic actinomycete , 1973 .

[41]  D. Kluepfel,et al.  Purification and properties of a xylanase from Streptomyces lividans. , 1986, The Biochemical journal.

[42]  P. Broda,et al.  Screening for lignin-degrading actinomycetes and characterization of their activity against [14C]lignin-labelled wheat lignocellulose , 1984 .

[43]  D. Crawford Lignocellulose decomposition by selected streptomyces strains , 1978, Applied and environmental microbiology.

[44]  F. Stutzenberger,et al.  Cellulolytic activity in municipal solid waste composting. , 1970, Canadian journal of microbiology.

[45]  B. Montenecourt,et al.  Genetic Recombination and Transformation in Protoplasts of Thermomonospora fusca , 1985, Applied and environmental microbiology.

[46]  G. Shama,et al.  Novel ethanol fermentations from sugar cane and straw , 1987, Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences.

[47]  D. Eveleigh,et al.  A cellobiohydrolase from a thermophilic actinomycete,Microbispora bispora , 1984 .

[48]  M. Penninckx,et al.  Identification and evolution of the cellulolytic microflora present during composting of cattle manure: on the role of Actinomycetes sp. , 1984, Annales de microbiologie.

[49]  D. Crawford,et al.  Genetic manipulation of ligninolytic streptomyces and generation of improved lignin-to-chemical bioconversion strains , 1984 .

[50]  A. Humphrey,et al.  The beta-xylosidase of Thermomonospora. , 1985, Biotechnology and bioengineering.

[51]  T. Nakajima,et al.  Purification and some properties of an endo-1,4-(3-D-xylanase from Streptomyces sp. , 1984 .

[52]  R. Crawford,et al.  Degradation of methoxylated benzoic acids by a Nocardia from a lignin-rich environment: significance to lignin degradation and effect of chloro substituents. , 1973, Applied microbiology.

[53]  D. Wood,et al.  An electron microscope study of wheat straw composted as a substrate for the cultivation of the edible mushroom (Agaricus bisporus) , 1983 .

[54]  F. Stutzenberger,et al.  pH-dependent thermal activation of endo-1,4-β-glucanase in Thermomonospora curvata , 1986 .

[55]  H. Ikeda,et al.  Production of ‘hybrid’ antibiotics by genetic engineering , 1985, Nature.

[56]  F. Stutzenberger Cellulase production by Thermomonospora curvata isolated from municipal solid waste compost. , 1971, Applied microbiology.

[57]  A. Humphrey,et al.  Kinetic characterization of the extracellular xylanases of Thermomonospora sp. , 1985, Biotechnology and bioengineering.

[58]  V. Bisaria,et al.  Biodegradation of cellulosic materials: Substrates, microorganisms, enzymes and products , 1981 .

[59]  D. Kluepfel,et al.  Method for the rapid screening of cellulolytic streptomycetes and their mutants. , 1979, Canadian journal of microbiology.

[60]  G. Engelhardt,et al.  Bacterial degradation of model compounds for lignin and chlorophenol derived lignin bound residues , 1980 .

[61]  P F Strom,et al.  Effect of temperature on bacterial species diversity in thermophilic solid-waste composting , 1985, Applied and environmental microbiology.

[62]  J. Lacey Actinomycetes in soils, composts and fodders. , 1973, Society for Applied Bacteriology symposium series.

[63]  T. Cross,et al.  A Taxonomic Study of Thermomonospora and Other Monosporic Actinomycetes , 1984 .

[64]  A. Collmer,et al.  Cloning and Expression of a Thermomonospora YX Endocellulase Gene in E. coli , 1983, Bio/Technology.

[65]  B. Pettersson,et al.  A zymogram technique for the detection of carbohydrases. , 1973, Analytical biochemistry.

[66]  P. Biely Microbial xylanolytic systems , 1985 .

[67]  D. Crawford,et al.  Isolation of lignocellulose-decomposing actinomycetes and degradation of specifically 14C-labeled lignocelluloses by six selected Streptomyces strains. , 1979, Canadian journal of microbiology.

[68]  G. Maluszynska,et al.  A cellulolytic rumen bacterium, Micromonospora ruminantium sp.nov. , 1974, Journal of general microbiology.

[69]  J. L. Woods,et al.  Thermophilic Fermentation of Pig Faeces and Straw by Actinomycetes , 1977 .

[70]  F. Stutzenberger Cellulolytic activity of Thermomonospora curvata: optimal assay conditions, partial purification, and product of the cellulase. , 1972, Applied microbiology.

[71]  F. Stutzenberger,et al.  Cellulase biosynthesis in a catabolite repression-resistant mutant of Thermomonospora curvata , 1984, Applied and environmental microbiology.

[72]  J. Cullum,et al.  Cloning and expression of an extracellular-agarase from Streptomyces coelicolor A3(2) in Streptomyces lividans 66. , 1984, Gene.

[73]  F. Stutzenberger Degradation of cellulosic substances by Thermomonospora curvata , 1979 .

[74]  H. Schoemaker,et al.  On the mechanism of enzymatic lignin breakdown , 1985 .

[75]  F. Stutzenberger,et al.  Cellulase biosynthesis during degradation of cellulose derivatives by Thermomonospora curvata , 1986 .

[76]  K. Eriksson,et al.  Specific Enzymic Hydrolysis of the Xylan in a Spruce Holocellulose , 1970 .

[77]  D. Crawford,et al.  Production and Characterization of Polymeric Lignin Degradation Intermediates from Two Different Streptomyces spp , 1985, Applied and environmental microbiology.

[78]  E. Pye,et al.  Saccharification of cellolulose by the cellulolytic enzyme system of Thermonospora sp. I. Stability of cellulolytic activities with respect to time, temperature, and pH , 1980 .

[79]  T. Wood,et al.  The isolation, purification and properties of the cellobiohydrolase component of Penicillium funiculosum cellulase. , 1980, The Biochemical journal.

[80]  S. Williams,et al.  Studies on the ecology of actinomycetes in soil—VIII: Distribution and characteristics of acidophilic actinomycetes , 1975 .

[81]  D. Hopwood Genetic manipulation of Streptomyces : a laboratory manual , 1985 .

[82]  P. Sneath,et al.  Numerical classification of Streptomyces and related genera. , 1983, Journal of general microbiology.

[83]  M. Goodfellow,et al.  Ecology of actinomycetes. , 1983, Annual review of microbiology.

[84]  John Arul Phillips,et al.  Production of cellulases by Thermomonospora sp. , 1981 .

[85]  Norton Nelson,et al.  A PHOTOMETRIC ADAPTATION OF THE SOMOGYI METHOD FOR THE DETERMINATION OF GLUCOSE , 1944 .

[86]  D. Crawford,et al.  Effects of carbon and nitrogen supplementation on lignin and cellulose decomposition by a Streptomyces. , 1981, Canadian journal of microbiology.

[87]  S. Waksman,et al.  THERMOPHILIC DECOMPOSITION OF PLANT RESIDUES IN COMPOSTS BY PURE AND MIXED CULTURES OF MICROORGANISMS , 1939 .

[88]  P. Broda,et al.  Degradation of [14C]lignin-labelled wheat lignocellulose by white-rot fungi , 1984 .

[89]  A. Humphrey,et al.  Utilization of carbohydrates by Thermomonospora sp. Grown on glucose, cellobiose, and cellulose , 1981 .

[90]  L. Smillie,et al.  Production, characterization, and partial amino acid sequence of xylanase A from Schizophyllum commune , 1978, Applied and environmental microbiology.

[91]  W. H. Zyl A Study of the cellulases produced by three mesophilic actinomycetes grown on bagasse as substrate. , 1985 .

[92]  T. Imanaka,et al.  Self-cloning in Streptomyces griseus of an str gene cluster for streptomycin biosynthesis and streptomycin resistance , 1985, Journal of bacteriology.