BioEnergy Research

, Volume 6, Issue 3, pp 1063–1081 | Cite as

Overview of the Oldest Existing Set of Substrate-optimized Anaerobic Processes: Digestive Tracts

  • Jean-Jacques Godon
  • Laure Arcemisbéhère
  • Renaud Escudié
  • Jérôme Harmand
  • Edouard Miambi
  • Jean-Philippe Steyer


Over millions of years, living organisms have explored and optimized the digestion of a wide variety of substrates. Engineers who develop anaerobic digestion processes for waste treatment and energy production can learn much from this accumulated ‘experience’. The aim of this work is a survey based on the comparison of 190 digestive tracts (vertebrate and insect) considered as ‘reactors’ and their anaerobic processes. Within a digestive tract, each organ is modeled as a type of reactor (continuous stirred-tank, such reactors in series, plug-flow or batch) associated with chemical aspects such as pH or enzymes. Based on this analysis, each complete digestion process has been rebuilt and classified in accordance with basic structures which take into account the relative size of the different reactors. The results show that all animal digestive structures can be grouped within four basic types. Size and/or position in the structure of the different reactors (pre/post treatment and anaerobic microbial digestion) are closely correlated to the degradability of the feed (substrate). Major common features are: (i) grinding, (ii) an extreme pH compartment, and (iii) correlation between the size of the microbial compartment and the degradability of the feed. Thus, shared answers found by animals during their evolution can be a source of inspiration for engineers in designing optimal anaerobic processes.


Animal mimicry Anaerobic digestion Digestive tract Degradability 



The authors are grateful for financial support from the Agence Nationale de la Recherche (ANR), France, under grant No. ANR-09-BIOE-06 (DANAC project).


  1. 1.
    Deublein D, Steinhauser A (2008) Biogas from Waste and Renewable Resources. Wiley-VCH, WeinheimCrossRefGoogle Scholar
  2. 2.
    Bayane A, Guiot SR (2011) Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass. Rev Environ Sci Biotechnol 10:43–62CrossRefGoogle Scholar
  3. 3.
    Weimer PJ, Russell JB, Muck RE (2009) Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. Bioresour Technol 100:5323–5331PubMedCrossRefGoogle Scholar
  4. 4.
    Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848PubMedCrossRefGoogle Scholar
  5. 5.
    Brune A (1998) Termite guts : the world’s smallest bioreactors. Trends Biotechnol 16:16–21CrossRefGoogle Scholar
  6. 6.
    Caton JM, Hume ID (2000) Chemical reactors of the mammalian gastro-intestinal tract. J Mamm Biol 65:33–50Google Scholar
  7. 7.
    Levenspiel O (1972) Chemical Reaction Engineering, 2nd edn. John Wiley & Sons, New YorkGoogle Scholar
  8. 8.
    Novick A, Szilard L (1950) Description of the chemostat. Science 112:715–716PubMedCrossRefGoogle Scholar
  9. 9.
    Monod J (1950) La technique de la culture continue: théorie et applications. Ann Inst Pasteur 79:390–410Google Scholar
  10. 10.
    Klasing KC (1999) Avian gastrointestinal anatomy and physiology. Sem Avian Exotic Pet Med 8:42–50CrossRefGoogle Scholar
  11. 11.
    Bartz SH, Holldobler B (1982) Colony founding in myrmecocystus-mimicus wheeler (hymenoptera, formicidae) and the evolution of foundress-associations. Behav Ecol Sociobiol 10:137–147CrossRefGoogle Scholar
  12. 12.
    Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University Press, CambridgeGoogle Scholar
  13. 13.
    Terra WR (1990) Evolution of digestive systems of insects. Annu Rev Entomol 35:181–200CrossRefGoogle Scholar
  14. 14.
    Huang S-W, Zhang H-Y, Marshall S, Jackson TA (2010) The scarab gut: A potential bioreactor for bio-fuel production. Insect Sci 17:175–183CrossRefGoogle Scholar
  15. 15.
    Brune A, Kuhl M (1996) pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes. J Insect Physiol 42:1121–1127CrossRefGoogle Scholar
  16. 16.
    Monlau F, Barakat A, Trably E, Dumas C, Steyer J-P, Carrere H (2013) Lignocellulosic materials into biohydrogen and biomethane: impact of structural features and pretreatment. Crit Rev Environ Sci Technol 43:260–322CrossRefGoogle Scholar
  17. 17.
    Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78:393–427PubMedGoogle Scholar
  18. 18.
    Kock KH (2005) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I. Polar Biol 28:862–895CrossRefGoogle Scholar
  19. 19.
    Gehring WJ, Wehner R (1995) Heat-shock protein-synthesis and thermotolerance in cataglyphis, an ant from the Sahara Desert. PNAS 92:2994–2998PubMedCrossRefGoogle Scholar
  20. 20.
    Giordano D, Russo R, Di Prisco G, Verde C (2012) Molecular adaptations in Antarctic fish and marine microorganisms. Mar Genomics 6:1–6PubMedCrossRefGoogle Scholar
  21. 21.
    Freckleton RP, Harvey PH, Pagel M (2003) Bergmann’s rule and body size in mammals. Am Nat 161:821–825PubMedCrossRefGoogle Scholar
  22. 22.
    Morgavi DP, Sakurada M, Tomita Y, Onodera R (1994) Presence in rumen bacterial and protozoal populations of enzymes capable of degrading fungal cell-walls. Microbiology 140:631–636PubMedCrossRefGoogle Scholar
  23. 23.
    Scharf ME, Karl ZJ, Sethi A, Boucias DG (2011) Multiple levels of synergistic collaboration in termite lignocellulose digestion. PLOS One 6:e21709PubMedCrossRefGoogle Scholar
  24. 24.
    Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512PubMedCrossRefGoogle Scholar
  25. 25.
    Angel CR (1996) A review of ratite nutrition. Anim Feed Sci Technol 60:241–246CrossRefGoogle Scholar
  26. 26.
    Martensson PE, Nordoy ES, Blix AS (1994) Digestibility of krill (euphausia-superba and thysanoessa sp) in minke whales (balaenoptera-acutorostrata) and crab-eater seals (lobodon carcinophagus). Br J Nutr 72:713–716PubMedCrossRefGoogle Scholar
  27. 27.
    Inward DJG, Vogler AP, Eggleton P (2007) A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. Mol Phylogenet Evol 44:953–967PubMedCrossRefGoogle Scholar
  28. 28.
    Hirakawa HIR (2001) Coprophagy in leporids and other mammalian herbivores. Mamm Rev 31:61–80CrossRefGoogle Scholar
  29. 29.
    Daly H, Doyen J, Ehrlich P (1981) Introduction to insect biology and diversity. McGraw-Hill Kogakusha, Tokyo, p 564Google Scholar
  30. 30.
    Sakaguchi E (2003) Digestive strategies of small hindgut fermenters. Anim Sci J 74:327–337CrossRefGoogle Scholar
  31. 31.
    Flatt WP (2002) Animal needs and uses (comparative nutrition). In: Berdanier CD (ed) Handbook of nutrition and food. CRC Press, Boca Raton, pp 163–172Google Scholar
  32. 32.
    Brauman A (2000) Effect of gut transit and mound deposit on soil organic matter transformations in the soil feeding termite: a review. Eur J Soil Biol 36:117–125CrossRefGoogle Scholar
  33. 33.
    Vo TL, Mueller UG, Mikheyev AS (2009) Free-living fungal symbionts (Lepiotaceae) of fungus-growing ants (Attini: Formicidae). Mycologia 101:206–210PubMedCrossRefGoogle Scholar
  34. 34.
    Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae : Scolytinae and Platypodinae). Evolution 55:2011–2027PubMedGoogle Scholar
  35. 35.
    Terra WR, Ferreira C (1994) Insect digestive enzymes — properties, compartmentalization and function. Comp Biochem Physiol B 109:1–62CrossRefGoogle Scholar
  36. 36.
    Smith HF, Fisher RE, Everett ML, Thomas AD, Bollinger RR, Parker W (2009) Comparative anatomy and phylogenetic distribution of the mammalian cecal appendix. J Evol Biol 22:1984–1999PubMedCrossRefGoogle Scholar
  37. 37.
    Randal Bollinger R, Barbas AS, Bush EL, Lin SS, Parker W (2007) Biofilms in the large bowel suggest an apparent function of the human vermiform appendix. J Theor Biol 249:826–831PubMedCrossRefGoogle Scholar
  38. 38.
    Clauss M, Schwarm A, Ortmann S, Streich WJ, Hummel J (2007) A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores. Comp Biochem Physiol A 148:249–265CrossRefGoogle Scholar
  39. 39.
    Krockenberger AK, Hume ID (2007) A flexible digestive strategy accommodates the nutritional demands of reproduction in a free-living folivore, the koala (Phascolarctos cinereus). Funct Ecol 21:748–756CrossRefGoogle Scholar
  40. 40.
    Schaller GB, Hu JH, Pan WS, Zhu J (1985) The giant pandas of Wolong. Science 228:875–876CrossRefGoogle Scholar
  41. 41.
    Tracy RL, Walsberg GE (2001) Developmental and acclimatory contributions to water loss in a desert rodent: investigating the time course of adaptive change. J Comp Physiol B 171:669–679PubMedCrossRefGoogle Scholar
  42. 42.
    Abbassi-Guendouz A, Brockmann D, Trably E, Dumas C, Delgenes J-P, Steyer J-P, Escudie R (2012) Total solids content drives high solid anaerobic digestion via mass transfer limitation. Bioresour Technol 111:55–61PubMedCrossRefGoogle Scholar
  43. 43.
    Karthikeyan O, Visvanathan C (2012) Bio-energy recovery from high-solid organic substrates by dry anaerobic bio-conversion processes: a review. Rev Environ Sci BiotechnolGoogle Scholar
  44. 44.
    Snipes R, Kriete A (1991) Quantitative investigation of the area and volume in different compartments of the intestine of 18 mammalian species. J Mamm Biol 56:225–244Google Scholar
  45. 45.
    Clauss M, Hummel J (2005) The digestive performance of mammalian herbivores : why big may not be that much better. Mammal Rev 35:174–187CrossRefGoogle Scholar
  46. 46.
    Smith K, McCoy KD, Macpherson AJ (2007) Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 19:59–69PubMedCrossRefGoogle Scholar
  47. 47.
    Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Doré J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65:4799–4807PubMedGoogle Scholar
  48. 48.
    Shepherd ML, Swecker WS, Jensen RV, Ponder MA (2012) Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons. FEMS Microbiol Lett 326:62–68PubMedCrossRefGoogle Scholar
  49. 49.
    Monteils V, Cauquil L, Combes S, Godon J-J, Gidenne T (2008) Potential core species and satellite species in the bacterial community within the rabbit caecum. FEMS Microbiol Ecol 66:620–629PubMedCrossRefGoogle Scholar
  50. 50.
    Kim M, Morrison M, Yu Z (2011) Status of the phylogenetic diversity census of ruminal microbiomes. FEMS Microbiol Ecol 76:49–63PubMedCrossRefGoogle Scholar
  51. 51.
    Wei G, Lu H, Zhou Z, Xie H, Wang A, Nelson K, Zhao L (2007) The microbial community in the feces of the giant panda (Ailuropoda melanoleuca) as determined by PCR-TGGE profiling and clone library analysis. Microb Ecol 54:194–202PubMedCrossRefGoogle Scholar
  52. 52.
    Hongoh Y, Ohkuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44:231–242PubMedCrossRefGoogle Scholar
  53. 53.
    Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T et al (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59–65PubMedCrossRefGoogle Scholar
  54. 54.
    Zoetendal E, Akkermans A, De Vos W (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64:3854–3859PubMedGoogle Scholar
  55. 55.
    Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788PubMedCrossRefGoogle Scholar
  56. 56.
    Guard CL (1980) The reptilian digestive system; general characteristics. In: Schmidt-Nielsen K, Bolis L, Taylor CR (eds) Comparative physiology: primitive mammals. Cambridge University Press, Cambridge, pp 43–51Google Scholar
  57. 57.
    Clemens ET, Stevens CE, SouthwortH M (1975) Sites of organic-acid production and pattern of digesta movement in gastrointestinal tract of geese. J Nutr 105:1341–1350PubMedGoogle Scholar
  58. 58.
    Herd RM, Dawson TJ (1984) Fiber digestion in the emu, dromaius-novaehollandiae, a large bird with a simple gut and high-rates of passage. Physiol Zool 57:70–84Google Scholar
  59. 59.
    Mackie RI (1987) Microbial digestion of forages in herbivores. In: Hacker JB, Ternouth JH (eds) The nutrition of herbivores. Academic Press, Sydney, pp 233–265Google Scholar
  60. 60.
    McWhorter TJ, Martínez del Rio C (2000) Does gut function limit hummingbird food intake? Physiol Biochem Zool 73:313–324PubMedCrossRefGoogle Scholar
  61. 61.
    Dellow DW (1982) Studies on the nutrition of macropodine marsupials.3. the flow of digesta through the stomach and intestine of macropodines and sheep. Aust J Zool 30:751–765CrossRefGoogle Scholar
  62. 62.
    Faichney GJ, White GA (1988) Partition of organic-matter, fiber and protein digestion in ewes fed at a constant rate throughout gestation. Aust J Agric Res 39:493–504CrossRefGoogle Scholar
  63. 63.
    Heller R, Cercasov V, Vonengelhardt W (1986) Retention of fluid and particles in the digestive-tract of the llama (lama-guanacoe f-glama). Comp Biochem Physiol A 83:687–691PubMedCrossRefGoogle Scholar
  64. 64.
    Uden P, Rounsaville TR, Wiggans GR, Vansoest PJ (1982) The measurement of liquid and solid digesta retention in ruminants, equines and rabbits given timothy (phleum-pratense) hay. Br J Nutr 48:329–339PubMedCrossRefGoogle Scholar
  65. 65.
    Kayouli C, Jouany JP, Demeyer DI, Aliali, Taoueb H, Dardillat C (1993) Comparative-studies on the degradation and mean retention time of solid and liquid-phases in the forestomachs of dromedaries and sheep fed on low-quality roughages from Tunisia. Anim Feed Sci Technol 40:343–355CrossRefGoogle Scholar
  66. 66.
    Orton RK, Hume ID, Leng RA (1985) Effects of exercise and level of dietary-protein on digestive function in horses. Equine Vet J 17:386–390PubMedCrossRefGoogle Scholar
  67. 67.
    Barboza PS (1993) Digestive strategies of the wombats - feed-intake, fiber digestion, and digesta passage in 2 grazing marsupials with hindgut fermentation. Physiol Zool 66:983–999Google Scholar
  68. 68.
    Sakaguchi E, Itoh H, Uchida S, Horigome T (1987) Comparison of fiber digestion and digesta retention time between rabbits, guinea-pigs, rats and hamsters. Br J Nutr 58:149–158PubMedCrossRefGoogle Scholar
  69. 69.
    Clemens ET, Stevens CE (1980) A comparison of gastrointestinal transit-time in 10 species of mammal. J Agric Sci 94:735–737CrossRefGoogle Scholar
  70. 70.
    Sakaguchi E, Nabata A (1992) Comparison of fiber digestion and digesta retention time between nutrias (myocaster-coypus) and guinea-pigs (Cavia porcellus). Comp Biochem Physiol A 103:601–604CrossRefGoogle Scholar
  71. 71.
    Sakaguchi E, Ohmura S (1992) Fiber digestion and digesta retention time in guinea-pigs (cavia-porcellus), degus (octodon-degus) and leaf-eared mice (phyllotis-darwini). Comp Biochem Physiol A 103:787–791CrossRefGoogle Scholar
  72. 72.
    Sakaguchi E, Heller R, Becker G, Vonengelhardt W (1986) Retention of digesta in the gastrointestinal-tract of the guinea-pig. J Anim Physiol Anim Nutr 55:44–50CrossRefGoogle Scholar
  73. 73.
    Foley WJ, Hume ID (1987) Passage of digesta markers in 2 species of arboreal folivorous marsupials - the greater glider (Petauroides volans) and the brushtail possum (Trichosurus vulpecula). Physiol Zool 60:103–113Google Scholar
  74. 74.
    Wellard GA, Hume ID (1981) Digestion and digesta passage in the brushtail possum, trichosurus-vulpecula (kerr). Aust J Zool 29:157–166CrossRefGoogle Scholar
  75. 75.
    Sakaguchi E, Hume ID (1990) Digesta retention and fiber digestion in brushtail possums, ringtail possums and rabbits. Comp Biochem Physiol A 96:351–354PubMedCrossRefGoogle Scholar
  76. 76.
    Sakaguchi E, Kaizu K, Nakamichi M (1992) Fiber digestion and digesta retention from different physical forms of the feed in the rabbit. Comp Biochem Physiol A 102:559–563CrossRefGoogle Scholar
  77. 77.
    Cork SJ, Warner ACI (1983) The passage of digesta markers through the gut of a folivorous marsupial, the koala phascolarctos-cinereus. J Comp Physiol 152:43–51Google Scholar

Copyright information

© European Union 2013

Authors and Affiliations

  • Jean-Jacques Godon
    • 1
  • Laure Arcemisbéhère
    • 1
  • Renaud Escudié
    • 1
  • Jérôme Harmand
    • 1
  • Edouard Miambi
    • 2
  • Jean-Philippe Steyer
    • 1
  1. 1.INRA, UR0050, Laboratoire de Biotechnologie de l’EnvironnementNarbonneFrance
  2. 2.UMR211 – BIOEMCO, Equipe Interactions Biologiques dans les Sols, IBIOSUniversité Paris Est Créteil (U-PEC)CréteilFrance

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