Skip to main content

Advertisement

Log in

Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass

  • Reviews
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Herbivorous mammals and wood-eating insects are fairly effective in the digestion of plant polymers, such as lignocellulosics. In order to improve methane production from the lignocellulosic biomass, several kinds of anaerobic digestion processes derived from animal models have been devised. However, the rates of biodegradation occurring in the anaerobic bioreactors still remain lower than in animal guts. The effectiveness of the digestive systems of those animals results from the concerted action of the various enzymes (e.g. cellulases, xylanases, esterases, ligninases) produced in their guts as well as their integration with mechanical and chemical actions. Powerful pretreatment (prefermentation) operations are integrated to and support efficiently the microbial fermentation system, e.g. the rumination (i.e. mechanical) in ruminants and the secretion of endogenous cellulases (i.e. enzymatic) or the alkaline treatment (chemical) at mid-way in xylophagous insects. The oxygen gradients along the gastrointestinal tract may also stimulate the hydrolytic activities of some microbial populations. In addition, the solid retention time, the digesta flow and the removal of the end-products are well ordered to enable animals to thrive on a complex polymer such as lignocellulose. At the same time, technologies were developed to degrade lignocellulosic biomass, such as the rumen derived anaerobic digestion (RUDAD) process and the rumen simulating technique (RUSITEC), more elaborated and using rumen microbial consortia. Overall, they showed that the fermentation taking place in the rumen fermentation and even in the hindgut are biological processes that go beyond the limited environmental conditions generally found in anaerobic digesters. Hence, knowledge on herbivores' digestion mechanisms might be better exploited in the design and operation of anaerobic digesters. This literature review is a cross-analysis of the relevant information about the digestive strategies of herbivorous and wood-eating animals and the bioengineering techniques in lignocelluloses degradation. The aim is to highlight strategies of animals' digestion simulation for more effective anaerobic digestion of lignocellulosic compounds and other solid residues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams JJ, Pal G, Jia Z, Smith SP (2006) Mechanism of bacterial cell-surface attachment revealed by the structure of cellulosomal type II cohesin-dockerin complex. Proc Natl Acad Sci USA 103:305–310

    Article  CAS  Google Scholar 

  • Akin DE (1989) Histological and physical factors affecting digestibility of forages. Agron J 81:17–25

    Article  Google Scholar 

  • Akin DE, Benner R (1988) Degradation of polysaccharides and lignin by ruminal bacteria and fungi. Appl Environ Microbiol 54:1117–1125

    CAS  Google Scholar 

  • Akkada AR, Howard BH (1961) The biochemistry of rumen protozoa. 4. Decomposition of pectic substances. Biochem J 78:512–517

    CAS  Google Scholar 

  • Anderson GK, Sallis PJ, Uyanik S (2003) Anaerobic treatment processes. In: Horan NJ, Mara D (eds) Handbook of water and wastewater microbiology. Academic Press, London

    Google Scholar 

  • Arakawa G, Watanabe H, Yamasaki H, Maekawa H, Tokuda G (2009) Purification and molecular cloning of xylanases from the wood-feeding termite, coptotermes formosanus Shiraki. Biosci Biotechnol Biochem 73:710–718

    Article  CAS  Google Scholar 

  • Bae DH, Welch JG, Gilman BE (1983) Mastication and rumination in relation to body size of cattle. J Dairy Sci 66:2137–2141

    Article  CAS  Google Scholar 

  • Barnes SP, Keller J (2003) Cellulosic waste degradation by rumen-enhanced anaerobic digestion. In Water Sci Technol 48(4):155–162

    CAS  Google Scholar 

  • Bauchop T (1980) Scanning electron microscopy in the study of microbial digestion of plant fragments in the gut. In: Elwood DC, Hedger JN, Latham MJ, Lynchand JM, Slater JH (eds) Contemporary microbial ecology. Academic Press, New York, pp 101–110

    Google Scholar 

  • Bjornhag G (1994) Adaptation in the large intestine allowing small animals to eat fibrous foods. In: Chivers DJ, Langer P (eds) The digestive system of mammals: food, form and fonction. Cambridge Unibversity Press, Cambridge, pp 287–309

    Chapter  Google Scholar 

  • Bolzonella D, Battistoni P, Mata-Alvarez J, Cecchi F (2003) Anaerobic digestion of organic solid wastes: process behaviour in transient conditions. Water Sci Technol 48(4):1–8

    CAS  Google Scholar 

  • Brad T, Braster M, Van Breukelen BM, Van Straalen NM, Röling WFM (2008) Eukaryotic diversity in an anaerobic aquifer polluted with landfill leachate. Appl Environ Microbiol 74:3959–3968

    Article  CAS  Google Scholar 

  • Brauman A, Kane MD, Labat M, Breznak JA (1992) Genesis of acetate and methane by gut bacteria of nutritionally diverse termites. Science 257:1384–1387

    Article  CAS  Google Scholar 

  • Breznak J, Brune A (1994) Role of microorganisms in the digestion of lignocellulose by termites. Annu Rev Entomol 39:453–487

    Article  CAS  Google Scholar 

  • Brulc JM, Antonopoulos DA, Miller ME, Wilson MK, Yannarell AC, Dinsdale EA, Edwards RE, Frank ED, Emerson JB, Wacklin P, Coutinho PM, Henrissat B, Nelson KE, White BA (2009) Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases. Proc Natl Acad Sci 106:1948–1953

    Article  CAS  Google Scholar 

  • Brune A (1998) Termite guts: the world's smallest bioreactors. Trends Biotechnol 16:16–21

    Article  CAS  Google Scholar 

  • Brune A, Friedrich M (2000) Microecology of the termite gut: structure and function on a microscale. Curr Opin Microbiol 3:263–269

    Article  CAS  Google Scholar 

  • Brune A, Emerson D, Breznak JA (1995) The termite gut microflora as an oxygen sink: microelectrode determination of oxygen and pH gradients in guts of lower and higher termites. Appl Environ Microbiol 61:2681–2687

    CAS  Google Scholar 

  • Bryant MP (1959) Bacterial species of the rumen. Bacteriol Rev 23:125–153

    CAS  Google Scholar 

  • Cerrato-Sanchez M, Calsamiglia S, Ferret A (2007) Effects of time at suboptimal pH on rumen fermentation in a dual-flow continuous culture system. J Dairy Sci 90:1486–1492

    Article  CAS  Google Scholar 

  • Chesson A, Forsberg CW (1988) Polysaccharids degradation by rumen microorganisms. In: Hobson PN, Stewart CS (eds) The rumen microbial ecosystem. Elsevier, London, pp 251–284

    Google Scholar 

  • Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Phil Trans R Soc Lond B 345:101–118

    Article  CAS  Google Scholar 

  • Confer DR, Logan BE (1997) Molecular weight distribution of hydrolysis products during the biodegradation of model macromolecules in suspended and biofilm cultures. II. Dextran and dextrin. Water Res 31:2137–2145

    Article  CAS  Google Scholar 

  • Czerkawski JW (1990) Relation between bacterial colonisation of fibrous residues and digestibility of dry matter in the rumen simulation technique (Risitec). Biol Wastes 32:219–224

    Article  CAS  Google Scholar 

  • Czerkawski JW, Breckenridge G (1969) The effect of oxygen on fermentation of sucrose by rumen micro-organisms in vitro. Br J Nutr 23:67–80

    Article  CAS  Google Scholar 

  • Czerkawski JW, Breckenridge G (1977) Design and development of a long-term rumen simulation technique (Rusitec). Br J Nutr 38:371–384

    Article  CAS  Google Scholar 

  • Czerkawski JW, Cheng JK (1988) Compartmentation in the rumen. In: Hobson P (ed) The rumen microbial ecosystem. Elsevier, London, pp 361–385

    Google Scholar 

  • Dague RR, Habben CE, Pidaparti SR (1992) Initial studies on the anaerobic sequencing batch reactor. Water Sci Technol 26(11):2429–2432

    CAS  Google Scholar 

  • Dalhoff R, Rababah A, Sonakya V, Raizada N, Wilderer PA (2003) Membrane separation to improve degradation of road side grass by rumen enhanced solid incubation. Water Sci Technol 48(4):163–168

    CAS  Google Scholar 

  • Daly K, Stewart CS, Flint HJ, Shirazi-Beechey SP (2001) Bacterial diversity within the equine large intestine as revealed by molecular analysis of cloned 16S rRNA genes. FEMS Microbiol Ecol 38:141–151

    Article  CAS  Google Scholar 

  • Dehority BA (2002) Gastrointestinal tracts of herbivores, particularly the ruminant: anatomy, physiology and microbial digestion of plants. J Appl Anim Res 21:145–160

    Google Scholar 

  • Dehority BA (2003) Rumen microbiology. Nottingham University Press

  • Demeyer DI, Van Nevel CJ (1979) Effect of defaunation on the metabolism of rumen micro-organisms. Br J Nutr 42:515–524

    Article  CAS  Google Scholar 

  • Deublein D, Steinhauser A (2008) Biogas from waste and renewable resources: an introduction. Wiley

  • Dijkstra J, Tamminga S (1995) Simulation of the effects of diet on the contribution of rumen protozoa to degradation of fibre in the rumen. Br J Nutr 74:617–634

    Article  CAS  Google Scholar 

  • Doi RH (2008) Cellulases of mesophilic microorganisms: cellulosome and noncellulosome producers. Ann N Y Acad Sci 1125:267–279

    Article  CAS  Google Scholar 

  • Dyer BD (2002) Termite hindgut symbionts. In: Seckbach J (ed) Symbiosis: mechanisms and model systems. Kluwer, Dordrecht, pp 703–713

    Google Scholar 

  • Eloff AK, van Hoven W (1980) Intestinal protozoa of the African elephant Loxodonta africana (Blumenbach). S Afr J Zool 15:83–90

    Google Scholar 

  • Engelhardt WV, Hinderer S, Rechkemmer G, Becker G (1984) Urea secretion into the colon of sheep and goat. Q J Exp Physiol 69:469–475

    Google Scholar 

  • Fenchel T, Finlay BJ (1990) Anaerobic free-living protozoa: growth efficiencies and the structure of anaerobic communities. FEMS Microbiol Ecol 74:269–276

    Article  Google Scholar 

  • Flint HJ, Bayer EA (2008) Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. In Ann NY Acad Sci 280–288

  • Fonty G, Grenet E, Fevre M, Breton A, Gouet P (1988) Ecologie et fonctions des champignons anaérobies du rumen. Reprod Nutr Develop 28:1–18

    Article  Google Scholar 

  • Fonty G, Jouany J, Forano E, Gouet P (1995) L'ecosystème microbien du reticulo-rumen. In: Jarrige R, Ruckebusch Y, Demarquilly C, Farce M-H, Journet M (eds) Nutrition des ruminants domestiques, ingestion et digestion. INRA, Paris, pp 299–348

    Google Scholar 

  • Frandson RD, Wilke WL, Fails AD (2003) Anatomy and physiology of farm animals, 6th edn. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Frape D (2004) Equine nutrition and feeding, 3rd edn. Blackwell, Oxford

    Book  Google Scholar 

  • Fuchigami M, Senshu T, Horiguchi M (1989) A simple continuous culture system for rumen microbial digestion study and effects of defaunation and dilution rates. J Dairy Sci 72:3070–3078

    Article  CAS  Google Scholar 

  • Fujita A, Hojo M, Aoyagi T, Hayashi Y, Arakawa G, Tokuda G, Watanabe H (2010) Details of the digestive system in the midgut of Coptotermes formosanus Shiraki. J Wood Sci. doi:10.1007/s10086-009-1088-3

  • Geib S, Filley T, Hatcher P, Hoover K, Carlson J, del Mar Jimenez-Gasco M, Nakagawa-Izumi A, Sleighter R, Tien M (2008) Lignin degradation in wood-feeding insects. Proc Natl Acad Sci USA 105:12932–12937

    Article  CAS  Google Scholar 

  • Gijzen HJ (2002) Anaerobic digestion for sustainable development: a natural approach. Water Sci Technol 45(10):321–328

    Google Scholar 

  • Gijzen HJ, Lubberding HJ, Verhagen FJ, Zwart KB, Vogels GD (1987) Application of rumen microorganisms for an enhanced anaerobic degradation of solid organic waste materials. Biol Wastes 22:81–95

    Article  CAS  Google Scholar 

  • Gijzen HJ, Lubberding HJ, Gerhardus MJT, Vogels GD (1988) Contribution of rumen protozoa to fibre degradation and cellulase activity in vitro. FEMS Microbiol Lett 53:35–43

    Article  CAS  Google Scholar 

  • Hack PJ, Vellinga SH (1995) Process for the biological treatment of solid organic material. In Google patent, US Patent 005431819. Jul 11, 1995

  • Heath IB (1988) Gut fungi. Trends Ecol Evol 3:167–171

    Article  Google Scholar 

  • Hendriks AT, Zeeman G (2009) Pretreatments to enhance the digestibility of lignocellulosic biomass. Bioresour Technol 100:10–18

    Article  CAS  Google Scholar 

  • Hillman K, Williams AG, Lloyd D (1991) Evaluation of matrices in the rumen simulation technique (RUSITEC) for the maintenance of ciliate protozoa. Lett Appl Microbiol 12:129–132

    Article  Google Scholar 

  • Hino T, Sugiyama M, Okumura K (1993) Maintenance of protozoa and methanogens, and fiber digestion in rumen- simulating continuous culture. J Gen Appl Microbiol 39:35–45

    Article  Google Scholar 

  • Hofmann RR (1988) Anatomy of the gastro-intestinal tract. In: Church DC (ed) The ruminant animal-digestive physiology and nutrition. Prentice-Hall, Englewood Cliffs, pp 14–43

    Google Scholar 

  • Hogan M, Veivers PC, Slaytor M, Czolij RT (1988a) The site of cellulose breakdown in higher termites (Nasutitermes walkeri and Nasutitermes exitiosus). J Insect Physiol 34:891–899

    Article  CAS  Google Scholar 

  • Hogan ME, Schulz MW, Slaytor M, Czolij RT, O'Brien RW (1988b) Components of termite and protozoal cellulases from the lower termite, Coptotermes lacteus froggatt. Insect Biochem 18:45–51

    Article  CAS  Google Scholar 

  • Hongoh Y, Sato T, Noda S, Ui S, Kudo T, Ohkuma M (2007) Candidatus Symbiothrix dinenymphae: bristle-like Bacteroidales ectosymbionts of termite gut protists. Environ Microbiol 9:2631–2635

    Article  CAS  Google Scholar 

  • Hoover WH, Crooker BA, Sniffen CJ (1976) Effects of differential solid-liquid removal rates on protozoa numbers in continous cultures of rumen contents. J Anim Sci 43:528–534

    Google Scholar 

  • Horn MH, Messer KS (1992) Fish guts as chemical reactors: a model of the alimentary canals of marine herbivorous fishes. Mar Biol 113:527–535

    Article  Google Scholar 

  • Hu ZH, Wang G, Yu HQ (2004) Anaerobic degradation of cellulose by rumen microorganisms at various pH values. Biochem Eng J 21:59–62

    Article  CAS  Google Scholar 

  • Hu ZH, Yu HQ, Yue ZB, Harada H, Li YY (2007) Kinetic analysis of anaerobic digestion of cattail by rumen microbes in a modified UASB reactor. Biochem Eng J 37:219–225

    Article  CAS  Google Scholar 

  • Hume ID (1989) Invited perspectives in physiological zoology: optimal digestive strategies in mammalian herbivores. Physiol Zool 62:1145–1163

    Google Scholar 

  • Hume ID (1997) Fermentation in the hindgut of mammals. In: Mackie RI, White AB (eds) Gastrointest microbiol. Chapman and Hall, New York, pp 231–265

    Google Scholar 

  • Hume DI (2002) Digestive strategies of mammals. Acta Zool Sin 48:1–19

    CAS  Google Scholar 

  • Hungate RE (1950) The anaerobic mesophilic cellulolytic bacteria. Bacteriol Rev 14:1–49

    CAS  Google Scholar 

  • Hungate RE (1982) Methane formation and cellulose digestion—biochemical ecology and microbiology of the rumen ecosystem. Experientia 38:189–192

    Article  CAS  Google Scholar 

  • Hungate RE, Bryant MP, Mah RA (1964) The rumen bacteria and protozoa. Annu Rev Microbiol 18:131–166

    Article  CAS  Google Scholar 

  • Hungate RE, Smith W, Clarke RT (1966) Suitability of butyl rubber stoppers for closing anaerobic roll culture tubes. J Bacteriol 91:908–909

    CAS  Google Scholar 

  • Hyodo F, Tayasu I, Inoue T, Azuma J-I, Kudo T, Abe T (2003) Differential role of symbiotic fungi in lignin degradation and food provision for fungus-growing termites (Macrotermitinae: Isoptera). Funct Ecol 17:186–193

    Article  Google Scholar 

  • Johjima T, Taprab Y, Noparatnaraporn N, Kudo T, Ohkuma M (2006) Large-scale identification of transcripts expressed in a symbiotic fungus (Termitomyces) during plant biomass degradation. Appl Microbiol Biotechnol 73:195–203

    Article  CAS  Google Scholar 

  • Jumars PA (2000a) Animal guts as ideal chemical reactors: maximizing absorption rates. Am Nat 155:527–543

    Article  Google Scholar 

  • Jumars PA (2000b) Animal guts as nonideal chemical reactors: partial mixing and axial variation in absorption kinetics. Am Nat 155:544–555

    Article  Google Scholar 

  • Kane MD (1997) Microbial fermentation in insect guts. In: Mackie RI, White AB (eds) Gastrointestinal microbiology. Chapman and Hall, New York, pp 84–115

    Google Scholar 

  • Karagiannidis A, Bilitewski B, Tchobanoglous G, Themelis NJ, Wittmaier M, Tsatsarelis T (2008) Waste to energy: on the thermal treatment and energetic utilization of solid wastes. In: Golush T (ed) Waste management research trends. Nova Science Publishers, New York, pp 105–164

    Google Scholar 

  • Katsumata K, Jin Z, Hori K, Iiyama K (2007) Structural changes in lignin of tropical woods during digestion by termite, Cryptotermes brevis. J Wood Sci 53:419–426

    Article  CAS  Google Scholar 

  • Kivaisi AK, Eliapenda S (1995) Application of rumen microorganisms for enhanced anaerobic degradation of bagasse and maize bran. Biomass Bioenerg 8:45–50

    Article  Google Scholar 

  • Kivaisi AK, Mtila M (1998) Production of biogas from water hyacinth (Eichhornia crassipes) (Mart) (Solms) in a two-stage bioreactor. World J Microb Biot 14:125–131

    Article  CAS  Google Scholar 

  • Kleiber M, Cole HH, Mead SW (1943) Bloat in cattle and composition of rumen gases. J Dairy Sci 26:929–933

    Article  CAS  Google Scholar 

  • Konig H (2006) Bacillus species in the intestine of termites and other soil invertebrates. J Appl Microbiol 101:620–627

    Article  CAS  Google Scholar 

  • Koppolu A, Clements LD (2004) Ruminal waste stream as a source of industrial chemicals. Resour Conserv Recy 41:215–226

    Article  Google Scholar 

  • Kubler H (1996) Method and apparatus for anaerobic biological hydrolysis and for subsequent biomethanisation. In Google patent, US Patent 005529692. Jun 25, 1996

  • Lai PY, Tamashiro M, Fujii JK (1983) Abundance and distribution of the three species of symbiotic Protozoa in the hindgut of Coptotermes formosanus (Isoptera: Rhinotermitidae). Proc Haw Entomol Soc 24:271–276

    Google Scholar 

  • Lambert JE (1998) Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol Anthropol 7:8–20

    Article  Google Scholar 

  • Lamed RE, Bayer EA (1988) The cellulosome concept: exocellular/extracellular enzyme reactors centers for efficient bindind and cellulosis. In: Aubert JP, Beguin P, Millet J (eds) Biochemistry and genetics of cellulose degradation. Academic press, New York, pp 101–116

    Google Scholar 

  • Larue R, Yu Z, Parisi VA, Egan AR, Morrison M (2005) Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing. Environ Microbiol 7:530–543

    Article  CAS  Google Scholar 

  • Lee SS, Choi CK, Ahn BH, Moon YH, Kim CH, Ha JK (2004) In vitro stimulation of rumen microbial fermentation by a rumen anaerobic fungal culture. Ani Feed Sci Tech 115:215–226

    Article  CAS  Google Scholar 

  • Logan JD, Joern A, Wolesensky W (2003) Chemical reactor models of optimal digestion efficiency with constant foraging costs. Ecol Model 168:25–38

    Article  Google Scholar 

  • Martin MM, Martin JS (1978) Cellulose digestion in the midgut of the fungus-growing termite macrotermes natalensis: the role of acquired digestive enzymes. Science 199:1453–1455

    Article  CAS  Google Scholar 

  • Mata-Alvarez J (2002) Fundamentals of the anaerobic digestion process. In: Mata-Alvarez J (ed) Biomethanization of the organic fraction of municipal solid wastes. IWA Publishing, London, pp 1–18

    Google Scholar 

  • McAllister TA, Bae HD, Jones GA, Cheng KJ (1994) Microbial attachment and feed digestion in the rumen. J Anim Sci 72:3004–3018

    CAS  Google Scholar 

  • McCowan RP, Cheng KJ, Bailey CBM, Costerton JW (1978) Adhesion of bacteria to epithelial cell surfaces within the reticulo-rumen of cattle. Appl Environ Microbiol 35:149–155

    CAS  Google Scholar 

  • Miron J, Ben-Ghedalia D, Morrison M (2001) Invited review: adhesion mechanisms of rumen cellulolytic bacteria. J Dairy Sci 84:1294–1309

    Article  CAS  Google Scholar 

  • Moriya S, Dacks JB, Takagi A, Noda S, Ohkuma M, Doolittle WF, Kudo T (2003) Molecular phylogeny of three oxymonad genera: pyrsonympha, dinenympha and oxymonas. J Eukaryot Microbiol 50:190–197

    Article  Google Scholar 

  • Morvan B, Bonnemoy F, Fonty G, Gouet P (1996) Quantitative determination of H2-utilizing acetogenic and sulfate-reducing bacteria and methanogenic archaea from digestive tract of different mammals. Curr Microbiol 32:129–133

    Article  CAS  Google Scholar 

  • Mountfort DO, Campbell J, Clements KD (2002) Hindgut fermentation in three species of marine herbivorous fish. Appl Environ Microbiol 68:1374–1380

    Article  CAS  Google Scholar 

  • Muetzel S, Lawrence P, Hoffmann EM, Becker K (2009) Evaluation of a stratified continuous rumen incubation system. Anim Feed Sci Tech 151:32–43

    Article  CAS  Google Scholar 

  • Nair S, Kuang Y, Pullammanappallil P (2005) Enhanced degradation of waste grass clippings in one and two stage anaerobic systems. Environ Technol 26:1003–1011

    Article  CAS  Google Scholar 

  • Noirot C (1995) The gut of termites (Isoptera). Comparative anatomy, systematics, phylogeny. I. Lower Termites. Ann Soc Entomol Fr 31:197–226

    Google Scholar 

  • Noirot C, Noirot-Timothée C (1969) The digestive system. In: Krishna K, Weesner FM (eds) Biology of termites. Academic Press, New York, pp 49–88

    Google Scholar 

  • Odelson DA, Breznak JA (1983) Volatile fatty acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol 45:1602–1613

    CAS  Google Scholar 

  • Okwakol MJN (1980) Estimation of soil and organic matter consumption by termites of the genus Cubitermes. Afr J Ecol 18:127–131

    Article  Google Scholar 

  • Owens FN, Goetsch LA (1988) Ruminal fermentation. In: Church DC (ed) The ruminant animal, digestive physiology and nutrition. Prentice-Hall, Englewood Cliffs, pp 145–171

    Google Scholar 

  • Palmowski L, Muller J (1999) Influence of the size reduction of organic waste on their anaerobic digestion. Paper presented at: 2nd International Symposium on Anaerobic Digestion of Solid Waste, Barcelona, Spain

  • Paster BJ, Canale-Parola E (1982) Physiological diversity of rumen spirochetes. Appl Environ Microbiol 43:686–693

    CAS  Google Scholar 

  • Paster BJ, Dewhirst FE, Cooke SM, Fussing V, Poulsen LK, Breznak JA (1996) Phylogeny of not-yet-cultured spirochetes from termite guts. Appl Environ Microbiol 62:347–352

    CAS  Google Scholar 

  • Pauss A, Nyns EJ (1993) Past, present and future trends in anaerobic digestion applications. Biomass Bioenerg 4:263–270

    Article  CAS  Google Scholar 

  • Pell NA, Schofield P (1993) Microbial adhesion and degradation of plant cell walls. In: Jung HG, Buxton DR, Hatfield RD, Ralph J (eds) Forage cell wall structure and digestibility, American society of agronomy, pp 397–423

  • Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96

    Article  CAS  Google Scholar 

  • Poirot CCM, Van Alebeek GJWM, Keltjens JT, Vogels GD (1991) Identification of para-cresol as a growth factor for Methanoplanus endosymbiosus. Appl Environ Microbiol 57:976–980

    CAS  Google Scholar 

  • Priya M, Haridas A, Manilal VB (2008) Anaerobic protozoa and their growth in biomethanation systems. Biodegradation 19:179–185

    Article  CAS  Google Scholar 

  • Raizada N, Sonakya V, Dalhoff R, Hausner M, Wilderer PA (2003) Population dynamics of rumen microbes using modern techniques in rumen enhanced solid incubation. Water Sci Technol 48(4):113–119

    CAS  Google Scholar 

  • Reilly K, Attwood GT (1998) Detection of Clostridium proteoclasticum and closely related strains in the rumen by competitive PCR. Appl Environ Microbiol 64:907–913

    CAS  Google Scholar 

  • Rychlik JL, Russell JB (2002) Bacteriocin-like activity of Butyrivibrio fibrisolvens JL5 and its effect on other ruminal bacteria and ammonia production. Appl Environ Microbiol 68:1040–1046

    Article  CAS  Google Scholar 

  • Sakaguchi E (2003) Digestive strategies of small hindgut fermenters. Anim Sci J 74:327–337

    Article  Google Scholar 

  • Sanchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194

    Article  CAS  Google Scholar 

  • Savage DC (1986) Gastrointestinal microflora in mammalian nutrition. Annu Rev Nutr 6:155–178

    Article  CAS  Google Scholar 

  • Schäfer A, Konrad R, Kuhnigk T, Kampfer P, Hertel H, Konig H (1996) Hemicellulose-degrading bacteria and yeasts from the termite gut. J Appl Microbiol 80:471–478

    Article  Google Scholar 

  • Scharf M, Tartar A (2008) Termite digestomes as sources for novel lignocellulases. Biofuels Bioprod Bioref 2:540–552

    Article  CAS  Google Scholar 

  • Schnurer A, Schnurer J (2006) Fungal survival during anaerobic digestion of organic household waste. Waste Manag 26:1205–1211

    Article  CAS  Google Scholar 

  • Scott RI, Yarlett N, Hillman K, Williams AG, Lloyd D, Williams TN (1983) The presence of oxygen in rumen liquor and its effects on methanogenesis. J Appl Microbiol 55:143–149

    Article  Google Scholar 

  • Seon J, Creuly C, Duchez D, Pons A, Dussap CG (2003) Degradation of plant wastes by anaerobic process using rumen bacteria. Water Sci Technol 48(4):213–216

    CAS  Google Scholar 

  • Shinkai T, Ohji R, Matsumoto N, Kobayashi Y (2009) Fibrolytic capabilities of ruminal bacterium Fibrobacter succinogenes in relation to its phylogenetic grouping. FEMS Microbiol Lett 294:183–190

    Article  CAS  Google Scholar 

  • Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427

    CAS  Google Scholar 

  • Stevenson DM, Weimer PJ (2007) Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR. Appl Microbiol Biotechnol 75:165–174

    Article  CAS  Google Scholar 

  • Stewart SC, Bryant MP (1988) The rumen bacteria. In: Hobson P, Stewart SC (eds) The rumen microbial ecosystem. Elsevier, London, pp 21–75

    Google Scholar 

  • Taprab Y, Johjima T, Maeda Y, Moriya S, Trakulnaleamsai S, Noparatnaraporn N, Ohkuma M, Kudo T (2005) Symbiotic fungi produce laccases potentially involved in phenol degradation in fungus combs of fungus-growing termites in Thailand. Appl Environ Microbiol 71:7696–7704

    Article  CAS  Google Scholar 

  • Tartar A, Wheeler M, Zhou X, Coy M, Boucias D, Scharf M (2009) Parallel metatranscriptome analyses of host and symbiont gene expression in the gut of the termite Reticulitermes flavipes. Biotechnol Biofuels 2:25. doi:10.1186/1754-6834-2-25

    Article  CAS  Google Scholar 

  • Teather RM, Sauer FD (1988) A naturally compartmented rumen simulation system for the continuous culture of rumen bacteria and protozoa. J Dairy Sci 71:666–673

    Article  CAS  Google Scholar 

  • Todaka N, Moriya S, Saita K, Hondo T, Kiuchi I, Takasu H, Ohkuma M, Piero C, Hayashizaki Y, Kudo T (2007) Environmental cDNA analysis of the genes involved in lignocellulose digestion in the symbiotic protist community of Reticulitermes speratus. FEMS Microbiol Ecol 59:592–599

    Article  CAS  Google Scholar 

  • Todaka N, Lopez C, Inoue T, Saita K, Maruyama J, Arioka M, Kitamoto K, Kudo T, Moriya S (2009) Heterologous expression and characterization of an endoglucanase from a symbiotic protist of the lower termite, Reticulitermes speratus. Appl Biochem Biotech 160:1168–1178

    Article  CAS  Google Scholar 

  • Tokuda G (2004) Major alteration of the expression site of endogenous cellulases in members of an apical termite lineage. Mol Ecol 13:3219–3228

    Article  CAS  Google Scholar 

  • Tokuda G, Watanabe H (2007) Hidden cellulases in termites: revision of an old hypothesis. Biol Lett 3:336–339

    Article  CAS  Google Scholar 

  • Tokuda G, Lo N, Watanabe H, Slaytor M, Matsumoto T, Noda H (1999) Metazoan cellulase genes from termites: intron/exon structures and sites of expression. BB-Gene Struct Expr 1447:146–159

    CAS  Google Scholar 

  • Tokuda G, Nakamura T, Murakami R, Yamaoka I (2001) Morphology of the digestive system in the wood-feeding termite Nasutitermes takasagoensis (Shiraki) [Isoptera: Termitidae]. Zool Sci 18:869–877

    Article  Google Scholar 

  • Tokuda G, Saito H, Watanabe H (2002) A digestive [beta]-glucosidase from the salivary glands of the termite, Neotermes koshunensis (Shiraki): distribution, characterization and isolation of its precursor cDNA by 5′- and 3′-RACE amplifications with degenerate primers. Insect Biochem Molec 32:1681–1689

    Article  CAS  Google Scholar 

  • Tokuda G, Lo N, Watanabe H (2005) Marked variations in patterns of cellulase activity against crystalline- vs. carboxymethyl-cellulose in the digestive systems of diverse, wood-feeding termites. Physiol Entomol 30:372–380

    CAS  Google Scholar 

  • Tokuda G, Miyagi M, Makiya H, Watanabe H, Arakawa G (2009) Digestive [beta]-glucosidases from the wood-feeding higher termite, Nasutitermes takasagoensis: Intestinal distribution, molecular characterization, and alteration in sites of expression. Insect Biochem Molec 39:931–937

    Article  CAS  Google Scholar 

  • Tokura M, Ohkuma M, Kudo T (2000) Molecular phylogeny of methanogens associated with flagellated protists in the gut and with the gut epithelium of termites. FEMS Microbiol Ecol 33:233–240

    Article  CAS  Google Scholar 

  • Vandevivere P, De Baere L, Verstraete W (2002) Types of anaerobic digester for solid wastes. In: Mata-Alvarez J (ed) Biomethanization of the organic fraction of municipal solid wastes. IWA Publishing, London, pp 111–137

    Google Scholar 

  • Varma A, Kolli BK, Paul J, Saxena S, Konig H (1994) Lignocellulose degradation by microorganisms from termite hills and termite guts: a survey on the present state of art. FEMS Microbiol Rev 15:9–28

    Article  CAS  Google Scholar 

  • Veivers PC, O'Brien RW, Slaytor M (1980) The redox state of the gut of termites. J Insect Physiol 26:75–77

    Article  Google Scholar 

  • Warnecke F, Luginbuhl P, Ivanova N et al (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nature 450:560–565

    Article  CAS  Google Scholar 

  • Watanabe H, Tokuda G (2010) Cellulolytic systems in insects. Annu Rev Entomol 55:609–632

    Article  CAS  Google Scholar 

  • Watanabe H, Noda H, Tokuda G, Lo N (1998) A cellulase gene of termite origin. Nature 394:330–331

    Article  CAS  Google Scholar 

  • Weems WA (1987) Intestinal fluid flow: its production and control. In: Robinson LR (ed) Physiology of the gastrointestinal tract. Raven Press, New York, pp 571–593

    Google Scholar 

  • Weimer PJ, Russell JB, Muck RE (2009) Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. Bioresource Technol 100:5323–5331

    Article  CAS  Google Scholar 

  • Weller RA, Pilgrim AF (1974) Passage of protozoa and volatile fatty acids from the rumen of the sheep and from a continuous in vitro fermentation system. Br J Nutr 32:341–351

    Article  CAS  Google Scholar 

  • Wenzel M, Schonig I, Berchtold M, Kampfer P, Konig H (2002) Aerobic and facultatively anaerobic cellulolytic bacteria from the gut of the termite Zootermopsis angusticollis. J Appl Microbiol 92:32–40

    Article  CAS  Google Scholar 

  • Williams AG, Coleman GS (1985) Hemicellulose-degrading enzymes in rumen ciliate protozoa. Curr Microbiol 12:85–90

    Article  CAS  Google Scholar 

  • Williams AG, Orpin CG (1987) Glycoside hydrolase enzymes present in the zoospore and vegetative growth stages of the rumen fungi Neocallimastix patriciarum, Piromonas communis, and an unidentified isolate, grown on a range of carbohydrates. Can J Microbiol 33:427–434

    Article  CAS  Google Scholar 

  • Williams AG, Withers SE (1983) Bacillus spp. in the rumen ecosystem. Hemicellulose depolymerases and glycoside hydrolases of Bacillus spp. and rumen isolates grown under anaerobic conditions. J Appl Bacteriol 55:283–292

    CAS  Google Scholar 

  • Wilson DB (2008) Three microbial strategies for plant cell wall degradation. Ann NY Acad Sci 1125:289–297

    Article  CAS  Google Scholar 

  • Wood T, Johnson R (1986) The biology, physiology, and ecology of termites. In: Economic impact and control of social insects, Praeger, Santa Barbara, pp 1–68

  • Yamano H, Koike S, Kobayashi Y, Hata H (2008) Phylogenetic analysis of hindgut microbiota in Hokkaido native horses compared to light horses. Anim Sci J 79:234–242

    Article  CAS  Google Scholar 

  • Yokoyama MT, Johnson KA (1988) Microbiology of the rumen and intestine. In: Church DC (ed) The ruminant animal-digestive physiology and nutrition. Prentice-Hall, Englewood Cliffs, pp 125–144

    Google Scholar 

  • Zhang YHP, Lynd LR (2004) Toward an aggregated understanding of enzymatic hydrolysis of cellulose: noncomplexed cellulase systems. Biotechnol Bioeng 88:797–824

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the NRCan-AAFC-NRC-National Bioproducts Program (NBP). NRC paper No. 53325.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Serge R. Guiot.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bayané, A., Guiot, S.R. Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass. Rev Environ Sci Biotechnol 10, 43–62 (2011). https://doi.org/10.1007/s11157-010-9209-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-010-9209-4

Keywords

Navigation