A list of cellulolytic bacteria Page

This list contains all truly cellulolytic bacterial species described in the literature (I am aware of) as substantially hydrolyzing crystalline cellulose and/or fermenting crystalline cellulose as sole carbon source. "Substantial" hydrolysis means continuous hydrolysis of at least microcrystalline cellulose like Avicel, or better filter paper, cotton linters, bacterial cellulose or the like - this is more than just e.g. initial activity on Avicel (e.g. release of reducing equivalents). The species are arranged by a superposition of the phylogenetic tree derived from calculation of 16 S rRNA sequences with the ARB program package (go to the Microbiology homepage), and the new taxonomic system published in Bergey´s Manual of Systematic Bacteriology (Garrity, 2001). Such a list will never be complete. So if you have data on a bacterial species which clearly show, that it grows on crystalline cellulose, please let me know. Wolfgang H. Schwarz (e-mail)

 

Phylogeny			Genus		Species		Temp	Source		Co	Reference
Phylum Firmicutes, Class Clostridia, Order Clostridiales
Fam. Syntrophomonodaceae			Caldocellulosiruptor		saccharolyticus		h	hot spring		-	Rainey et al. 1994
			Caldocellulosiruptor		lactoaceticus		h				Mladenovska et al. 95
			Caldocellulosiruptor		kristjanssonii		h	hot spring		-	Bredholt et al., 1999
			"Anaerocellum"		thermophilum		h			-	Svetlichnyi et al. 1990
Fam. Lachnospiraceae			Butyrivibrio		fibrisolvens		m	rumen		+	Berger et al. 1990
			Ruminococcus		flavefaciens		m	rumen		+a,b	Aurilia et al. 2000
			Ruminococcus		succinogenes		m	rumen			Fields et al. 2000
			Ruminococcus		albus		m	rumen		+a,b	Ohara et al. 2000
Fam. Eubacteriaceae			Eubacterium		cellulolyticum		m	rumen			Anderson & Blair 96
Fam. Clostridiaceae			Clostridium		acetobutylicum		m	soil		(+)a	From sequence
			Clostridium		chartatabidum		m	rumen			Kelly et al. 1987
			Clostridium		cellulovorans		m	wood fermenter		+a,b	Shoseyov et al. 1992, Tamaru et al. 2000
			Clostridium		herbivorans		m	pig intestine			Varel et al. 1995
			Clostridium		cellulosi		h	manure			Yanling et al. 1991
			Clostridium		cellobioparum		m	rumen		+b	Lamed et al. 1987
			Clostridium		papyrosolvens		m	paper mill		+c	Pohlschröder et al. 94
			Clostridium		josui		h	compost		+a	Kakiuchi et al., 1998
			Clostridium		cellulolyticum		m	compost		+a,b	Pagés et al. 1997, Belaich et al. 1997
			Clostridium		aldrichii		m	wood fermenter			Yang et al. 1990
			Clostridium		stercorarium		h	compost		-	Schwarz et al. 1995
			Clostridium		thermocellum		h	sewage + soil		+a,b	Lamed et al. 1991
			Clostridium		cellulofermentans		m	manure			Yanling et al. 1991
			Clostridium		celerescens		m	manure			Palop et al. 1989
			Clostridium		thermopapyrolyticum		h	mud			Mendez et al. 1991
			Clostridium		thermocopriae		h	hot spring			Jin & Toda 1989
			Clostridium		sp. C7		m	mud		+b,d	Cavedon et al. 1990
			Bacteroides		sp. P-1		h	rotting biomass		+b	Ponpium et al. 2000
			Bacteroides		cellulosolvens		m	sewage		+a,c	Lamed et al. 1991
			Acetivibrio		cellulolyticus		m	sewage		+a,b	Ding et al. 1999
			Acetivibrio		cellulosolvens		m	sewage			Khan et al. 1984
Phylum Firmicutes, Class Bacilli, Order Bacillales
Fam. Thermoactinomycetaceae			Thermoactinomyces		sp. YX		h				Hägerdahl et al., 1979
			Caldibacillus		cellulovorans		h				Sunna et al. 2000
Fam. Bacillaceae			Bacillus		circulans		m				Kim 1995
Phylum Actinobacteria, Order Actinomycetales
Subord. Frankineae, Fam. Acidothermaceae			Acidothermus		cellulolyticus		h	acidic hot spring		-	Eppard et al. 1996; Maréchal et al. 2000
			Cellulomonas		biazotea		m				Lednicka et al 2000
Subord. Micromonosporineae, Fam. Cellulomonadaceae			Cellulomonas		cartae		m				Thayer et al. 1984
			Cellulomonas		cellasea		m				Lednicka et al. 2000
			Cellulomonas		cellulans		m	soil			Lednicka et al. 2000
			Cellulomonas		fimi		m	soil		-	Lednicka et al. 2000
			Cellulomonas		flavigena		m	soil			Lednicka et al. 2000
			Cellulomonas		gelida		m				Thayer et al. 1984
			Cellulomonas		iranensis		m	forest soil		-	Elberson et al. 2000
			Cellulomonas		persica		m	forest soil		-	Elberson et al. 2000
			Cellulomonas		uda		m	sewage		-	Thayer et al. 1984
			Curtobacterium		falcumfaciens		m	soil			Lednicka et al. 2000
Fam. Microbacteriaceae			Micromonospora		melonosporea		m	compost			Wilson 1992
Fam. Micromonosporaceae			Actinoplanes		aurantiaca		m	soil			Coughlan & Mayer 92
			Streptomyces		reticuli		m	soil			Schrempf & Walter 96
Suborder Streptomycineae, Fam. Streptomycetaceae			Streptomyces		alboguseolus		m				Van Zyl 1985
			Streptomyces		aureofaciens		m	compost			El-Din et al. 2000
			Streptomyces		cellulolyticus		m				Li 1997
			Streptomyces		flavogriseus		m	soil			MacKenzie et al. 1984
			Streptomyces		lividans		m				Kluepfel et al. 1986
			Streptomyces		nitrosporeus		m				Van Zyl 1985
			Streptomyces		olivochromogenes						Coughlan & Mayer 92
			Streptomyces		rochei		m	termite gut			Perito et al. 1994
			Streptomyces		thermovulgaris						Coughlan & Mayer 92
			Streptomyces		viridosporus						Coughlan & Mayer 92
Subord. Streptosporangiaceae, Fam. Nocardiopsaceae			Thermobifida		alba		m				Kukolya, pers. commun.
			Thermobifida (Thermomonospora)		fusca		h	soil		d	Wilson 1992; Kukolya, pers. commun. 2003
			Thermobifida		cellulolytica		h	compost			Kukolya et al. 2002
			Thermomonospora		curvata		h				Coughlan & Mayer 92
			Microbispora		bispora		h	soil			Wilson 1992
Fam. Streptosporangiaceae
Phylum Fibrobacteres, Class Fibrobacteres, Order Fibrobacterales
Fam. Fibrobacteriaceae			Fibrobacter		succinogenes		m	rumen		+d	Schellhorn & Forsberg 1984
Phylum Bacteroidetes, Class Sphingobacteria, Order Sphingobacteriales
Fam. Flexibacteriaceae			Sporocytophaga		myxococcoides		m	soil			Coughlan & Mayer 92
			Cytophaga		sp.		m	soil			Mullings et al. 1984
Phylum Bacteroidetes, Class Flavobacteria, Order Flavobacteriales
Fam. Flavobacteriaceae			Flavobacterium		johnsoniae		m	soil			Lednicka et al. 2000
Phylum Proteobacteria, Class Betaproteobacteria, Order Burkholderiales
Fam. Alcaligenaceae			Achromobacter		piechaudii		m	soil			Lednicka et al. 2000
Phylum Proteobacteria, Class Gammaproteobacteria, Order Xanthomonadales
Fam. Xanthomonadaceae			Xanthomonas		sp.		m	brack water			Mullings et al. 1984
Phylum Proteobacteria, Class Gammaproteobacteria, Order Pseudomonadales
Fam. Pseudomonaceae			Cellvibrio		vulgaris, fulvus		m	soil			Blackall et al. 1985
			Cellvibrio		gilvus		m	soil			Coughlan & Mayer 92
			Cellvibrio		mixtus		m	soil			Lednicka et al. 2000
			Pseudomonas		fluorescens (cellulosa)		m	plant pathogen		-	Dees et al. 1995
			Pseudomonas		mendocina		m	soil			Lednicka et al. 2000
Phylum Proteobacteria, Class Deltaproteobacteria
Fam. unclassified			Myxobacter		sp. AL-1		m	soil			Avitia et al. 2000, Pedraza-Reyes (pers. commun.)

Last update 24.04.2003, © W. Schwarz, TUM, Microbiology

Legend: Temp, growth temperature: m, mesophilic; h, thermophilic (growth optimum above 50 °C). Co, presence of cellulosomes; evidence: a) presence of dockerin of cohesin sequences; b) biochemical evidence (multienzyme complexes); c) reaction with Ct-CipA-scaffoldin antibodies; d) presence of cell protuberances in electron microscopy.

 

Acknowledgements: I thank all collegues who contributed to this page for personal communication of unpublished results.

 

References:

A number of reviews has been published recently giving an overview: 

 

1. Bayer EA, Morag E, Lamed R, Yaron S, Shoham Y (1998) Cellulosome structure: four-pronged attack using biochemistry, molecular biology, crystallography and bioinformatics. In Carbohydrates from Trichoderma reesei and other microorganisms. (M. Claeyssens, W. Nerinckx and K. Piens, eds.). pp. 39-65. The Royal Society of Chemistry, London
2. Coughlan MP, Mayer F (1992) The cellulose-decomposing bacteria and their enzyme systems. In The Prokaryotes: a handbook on the biology of bacteria. 2ns edn., p. 460-516. Edited by Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH. Springer-Verlag, New York
3. Doi RH, Goldstein M, Hashida S, Park JS, Takagi M (1994) The Clostridium cellulovorans cellulosome. Crit Rev Microbiol 20: 87-93
4. Doi RH, Park JS, Liu CC, Malburg LM, Tamaru Y, Ichiishi A, Ibrahim A (1998) Cellulosome and noncellulosomal cellulases of Clostridium cellulovorans. Extremophiles 2: 53-60
5. Gal L, Pagés S, Gaudin C, Belaich A, Reverbel-leroy C, Tardif C, Belaich JP (1997) Characterization of the cellulolytic complex (cellulosome) produced by Clostridium cellulolyticum. Appl Environ Microbiol 63: 903-909
6. Guglielmi G, Béguin P (1998) Cellulase and hemicellulase genes of Clostridium thermocellum from five independent collections contain few overlaps and are widely scattered across the chromosome. FEMS Microbiol Let 161: 209-215
7. Himmel ME, Ruth MF, Wyman CE (1999) Cellulase for commodity products from cellulosic biomass. Curr Opin Biotechnol 10: 358-364
8. Karita S, Sakka K, Ohmiya K (1997) Cellulosomes, cellulase complexes, of anaerobic microbes: their structure, models and functions. In Rumen Microbes and Digestive Physiology in Ruminants, Onodera R et al. eds., pp. 47-57. Japan Sci. Soc. Press, Tokyo/S. Karger, Basel.
9. Schülein M (2000) Protein engineering of cellulases. Biochim Biophys Acta 1543: 239-252
10. Sheehan J, Himmel M (1999) Enzymes, energy, and the environment: a strategic perspective on the U.S. department of energy´s research and development activities for bioethanol. Biotechnol Prog 15: 817-827
11. Shoham Y, Lamed R, Bayer EA (1999) The cellulosome concept as an efficient microbial strategy for the polysaccharide degradation of insoluble polysaccharides. Trends Microbiol 7: 275-281
12. Tomme P, Boraston A, McLean B, Kormos J, Creagh AL, Sturch K, Gilkes NR, Haynes CA, Warren RAJ, Kilburn DG (1998) Characterization and affinity applications of cellulose-binding domains. J Chromatogr B 715: 283-296
13. Tomme P, Warren RA, Miller RC Jr, Kilburn DG, Gilkes,N (1995) In: Enzymatic Degradation of Insoluble Polysaccharides (Saddler, J.N. & Penner, M., eds.), Cellulose-binding domains: classification and properties. pp. 142-163, American Chemical Society, Washington

     

    A server containing all known cellulase sequences, grouped in families. It is continuously updated: 

14. Coutinho, P.M. & Henrissat, B. (1999) Carbohydrate-Active Enzymes server at
    URL: http://afmb.cnrs-mrs.fr/~cazy/CAZY/index.html
15. Henrissat B, Teeri TT, Warren RAJ (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Let 425: 352-354
16. Henrissat B., Bairoch A. (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316: 695-696.

     

These references cite the paper where the cellulolytic trait was described: 

1. Anderson KL, Blair BG (1996) Regulation of the cellulolytic activity of Eubacterium cellulosolvens 5494: a review. SAAS Bull Biochem Biotechnol 9: 57-62
2. Aurilia V, Martin JC, McCrae SI, Scot KP, Rincon MT, Flint HJ (2000) Three multidomain esterases from the cellulolytic rumen anaerobe Ruminococcus flavefaciens 17 that carry divergent dockerin sequences. Microbiol 146: 1391-1397 
3. Avitia CI, Castellanos-Juarez FX, Sanchez E, Tellez-Valencia A, Fajardo-Cavazos P, Nicholson WL, Pedraza-Reyes M (2000) Temporal secretion of a multicellulolytic system in myxobacter sp. AL-1 molecular cloning and heterologous expression of cel9 encoding a modular endocellulase clustered in an operon with cel48, an exocellobiohydrolase gene. Eur J Biochem. 267:7058-64
4. Bélaich JP, Tardif C, Bélaich A, Gaudin C (1997) The cellulolytic system of Clostridium cellulolyticum. J Biotechnol 57: 3-14
5. Berger E, Jones WA, Jones DT, Woods DR (1990) Sequencing and expression of a cellodextrinase (ced1) gene from Butyrivibrio fibrisolvens H17c cloned in Escherichia coli. Mol Gen Genet 223: 310-318
6. Blackall LL, Hayward AC, Sly LI (1985) Cellulolytic and extremophilic Gram-negative bacteria: revival of the genus Cellvibrio. J Appl Bacteriol 59: 81-97
7. Bredholt S, Sonne-Hansen J, Nielsen P, Mathrani IM, Ahring BK (1999) Caldicellulosiruptor kristjanssonii sp. nov., a cellulolytic, extremely thermophilic, anaerobic bacterium. Int J Syst Bacteriol 49: 991-996
8. Cavedon K, Leschine SB, Canale-Parola E (1990) Cellulase system of a free-living, mesophilic Clostridium (strain C7). J Bacteriol 172: 4222-4230
9. Coughlan MP, Mayer F (1992) The cellulose-decomposing bacteria and their enzyme systems. In The Prokaryotes: a handbook on the biology of bacteria. 2ns edn., p. 460-516. Edited by Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH. Springer-Verlag, New York
10. Dees C, Ringelberg D, Scott TC, Phelps TJ (1995) Characterization of the cellulose degrading bacterium NCIMB 10462. Appl Biochem Biotechnol 51: 263-274
11. Ding SY, Bayer EA, Steiner D, Shoham Y, Lamed R (1999) A novel cellulosomal scaffoldin from Acetivibrio cellulolyticus that contains a family 9 glycosyl hydrolase. J Bacteriol 181: 6720-6729
12. Elberson MA, Malekzadeh F, Yazdi MT, Kameranpour N, Noori-Dloii MR, Matte MH, Shahamat M, Colwell RR, Sowers KR (2000) Cellulomonas persica sp. nov. and Cellulomonas iranensis sp. nov., mesophilic cellulose-degrading bacteria isolated from forest soil. Int J System Evol Microbiol 50: 993-996
13. Eppard M, Krumbein WE, Koch C, Rhiel E, Staley JT, Stackebrandt E (1996) Morphological, physiological, and molecular characterization of Actinomycetes isolated from dry soil, rocks, and monument surfaces. Arch Microbiol. 166:12-22
14. Fields MW, Mallik S, Russell JB (2000) Fibrobacter succinogenes S85 ferments ball-milled cellulose as fast as cellobiose until cellulose surface area is limiting. Appl Microbiol Biotechnol 54: 570-574
15. Garrity GM ed. (2001) Bergey´s manual of systematic bacteriology. 2^nd ed.. Springer-Verlag New York
16. Hägerdahl B, Harris H, Pye EK (1979) Association of beta-glucosidase with intact cells of Thermoactinomyces.
    Biotechnol Bioeng 21: 345-55
17. Jin F, Toda K (1989) Purification and characterization of cellulases from Clostridium thermocopriae sp. nov. JT3-3. J Ferment Bioeng 67: 8-13
18. Kakiuchi M, Isui A, Suzuki K, Fujino T, Fujino E, Kimura T, Karita S, Sakka K, Ohmiya K (1998) Cloning and DNA sequencing of the genes encoding Clostridium josui scaffolding protein CipA and cellulase CelD and identification of their gene products as major components of the cellulosome. J Bacteriol 180: 4303-4308
19. Kelly WJ, Asmundson RV, Hopcroft DH (1987) Isolation and characterization of a strictly anaerobic, cellulolytic spore former: Clostridium chartatabidum sp. nov. Arch Microbiol 147: 169-173
20. Khan AW, Meek E, Sowden LC, Colden JR (1984) Emendation of the genus Acetivibrio and description of Acetivibrio cellulosolvens sp. nov., a nonmotile celluloytic mesophile. Int J Syt Bacteriol 34: 419-422
21. Kim CH (1995) Characterization and substrate specificity of an endo-ß-1,4-D-glucanase I (Avicelase I) from an extracellular multienzyme complex of Bacillus circulans. Appl Environ Microbiol 61: 959-965
22. Lamed R, Naimark J, Morgenstern E, Bayer EA (1987) Specialized surface structure in cellulolytic bacteria. J Bacteriol 169: 3792-3800
23. Lamed R, Morag E, Moryosef O, Bayer EA (1991) Cellulosome-like entities in Bacteroides cellulosolvens. Curr Microbiol 22: 27-34
24. Lednicka D, Mergaert J, Cnockaert MC, Swings J (2000) Isolation and identification of cellulolytic bacteria involved in the degradation of natural cellulosic fibres. Syst Appl Microbiol. 23:292-299
25. Li X, Chen H, Ljungdahl L (1997) Appl Environ Microbiol 63: 4721-4728
26. MacKenzie CR, Bilous D, Johnson KG (1984) Purification and characterization of an exoglucanase from Streptomyces flavogriseus. Can J Microbiol 30: 1171-1178
27. Méndez BS, Pettinari MJ, Ivanier SE, Ramos CA, Sineriz F (1991) Clostridium thermopapyrolyticum sp. nov., a cellulolytic thermophile. Int J Syst Bacteriol 41: 281-283
28. Mladenovska Z, Mathrani IM, Ahring BK (1995) Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an extremely thermophilic, cellulolytic anaerobic bacterium. Arch Microbiol 163: 223-230
29. Mullings R, Parish JH (1984) Mesophilic aerobic Gram negative cellulose degrading bacteria from aquatic habitats and soils. J Appl Bacteriol 57: 455-468
30. Ohara H, Karita S, Kimura T, Sakka K, Ohmiya K (2000) Characterization of the cellulolytic complex (cellulosome) from Ruminococcus albus. Biosci Biotechnol Biochem 64: 254-260
31. Pagés S, Gal L, Bélaich A, Gaudin C, Tardif C, Bélaich JP (1997) Role of scaffolding protein CipC of Clostridium cellulolyticum in cellulose degradation. J Bacteriol 179: 2810-2816
32. Palop ML, Valles S, Pinaga F, Flors A (1989) Isolation and characterization of an anaerobic, cellulolytic bacterium, Clostridium celerescens sp. nov. Int J Syst Bacteriol 39: 68-71
33. Perito B, Hanhart E, Irdani T, Iqbal M, McCarthy AJ, Mastromei G (1994) Characterization and sequence analysis of a Streptomyces rochei A2 endoglucanase-encoding gene. Gene. 148:119-24
34. Pohlschröder M, Canale-Parola E, Leschine SB (1995) Ultrastructural diversity of the cellulase complexes of Clostridium papyrosolvens C7. J Bacteriol 177: 6625-6629
35. Ponpium P, Ratanakhanokchai K, Kyu KL (2000) Isolation and properties of a cellulosome-type multienzyme complex of the thermophilic Bacteroides sp. strain P-1. Enz Microb Technol 26: 459-465
36. Rainey FA, Donnison AM, Janssen PH, Saul D, Rodrigo A, Bergquist PL, Daniel RM, Stackebrandt E, Morgan HW (1994) Description of Caldicellulosiruptor saccharolyticus gen. nov., sp. nov.: an obligately anaerobic, extremely thermophilic, cellulolytic bacterium. FEMS Microbiol Let 120: 263-266
37. Schellhorn HE, Forsberg CW (1984) Multiplicity of extracellular ß-(1,4)-endoglucanases of Bacteroides succinogenes S85. Can J Microbiol 30: 930-937
38. Schrempf H, Walter S (1995) The cellulolytic system of Streptomyces reticuli.
    Int J Biol Macromol. 17:353-355
39. Schwarz WH, Bronnenmeier K, Landmann B, Wanner G, Staudenbauer WL, Kurose N, Takayama T (1995) Molecular characterization of four strains of the cellulolytic thermophile Clostridium stercorarium. Biosci Biotech Biochem 59: 1661-1665
40. Shoseyov O, Doi RH (1990) Essential 170-kDa subunit for degradation of crystalline cellulose by Clostridium cellulovorans cellulase. Proc Natl Acad Sci USA 87: 2192-2195
41. Sunna A, Gibbs MD, Chin CW, Nelson PJ, Bergquist PL (2000) A gene encoding a novel multidomain beta-1,4-mannanase from Caldibacillus cellulovorans and action of the recombinant enzyme on kraft pulp. Appl Environ Microbiol. 66:664-70
42. Svetlichnyi VA, Svetlichnaya TP, Chernykh NA, Zavarzin GA (1990) Anaerocellum thermophilum gen. nov., sp. nov.: an extremely thermophilic cellulolytic eubacterium isolated from hot springs in the valley of geysers. Microbiol (Rus.) 59: 598-604
43. Tamaru Y, Karita S, Ibrahim A, Chan H, Doi RH (2000) A large gene cluster for the Clostridium cellulovorans cellulosome. J Bacteriol 182: 5906-5910
44. Thayer DW, Lowther SV, Phillips JG (1984) Cellulolytic activities of the genus Cellulomonas. Int J Syst Bacteriol 34: 432-438
45. Varel VH, Yen JT, Kreikemeier KK (1995) Addition of cellulolytic clostridia to the bovine rumen and pig intestinal tract. Appl Environ Microbiol. 61: 1116-1119
46. Wilson DB (1992) Biochemistry and genetics of actinomycete cellulases.
    Crit Rev Biotechnol. 12:45-63
47. Yang JC, Chynoweth DP, Williams DS, Li A (1990) Clostridium aldrichii sp. nov., a cellulolytic mesophile inhabiting a wood-fermenting anaerobic digester. Int J Syst Bacteriol 40: 268-272
48. Yanling H, Youfang D, Yanquan L (1991) Two cellulolytic Clostridium species: Clostridium cellulosi sp. nov. and Clostridium cellulofermentans sp. nov. (1991) Int J Syst Bacteriol 41: 306-309