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

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.

[1]  R. Heller,et al.  Retention of fluid and particles in the digestive tract of the llama (Lama guanacoe f. glama). , 1986, Comparative biochemistry and physiology. A, Comparative physiology.

[2]  R. Ley,et al.  Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine , 2006, Cell.

[3]  Chettiyappan Visvanathan,et al.  Bio-energy recovery from high-solid organic substrates by dry anaerobic bio-conversion processes: a review , 2013, Reviews in Environmental Science and Bio/Technology.

[4]  C. R. Taylor,et al.  Comparative Physiology: Primitive Mammals , 2009 .

[5]  A. Warner,et al.  The passage of digesta markers through the gut of a folivorous marsupial, the koalaPhascolarctos cinereus , 1983, Journal of comparative physiology.

[6]  W. Foley,et al.  Passage of Digesta Markers in Two Species of Arboreal Folivorous Marsupials: The Greater Glider (Petauroides volans) and the Brushtail Possum (Trichosurus vulpecula) , 1987, Physiological Zoology.

[7]  K. Klasing Avian gastrointestinal anatomy and physiology , 1999 .

[8]  W. Terra Evolution of Digestive Systems of Insects , 1990 .

[9]  G. Faichney,et al.  Partition of organic matter, fibre and protein digestion in ewes fed at a constant rate throughout gestation , 1988 .

[10]  D. Deublein,et al.  Biogas from Waste and Renewable Resources , 2008 .

[11]  C. Verde,et al.  Molecular adaptations in Antarctic fish and marine microorganisms. , 2012, Marine genomics.

[12]  W. Terra,et al.  Insect digestive enzymes: properties, compartmentalization and function , 1994 .

[13]  Y. Tomita,et al.  Presence in rumen bacterial and protozoal populations of enzymes capable of degrading fungal cell walls. , 1994, Microbiology.

[14]  Shu-sen Lin,et al.  Biofilms in the large bowel suggest an apparent function of the human vermiform appendix. , 2007, Journal of theoretical biology.

[15]  I. Hume,et al.  A flexible digestive strategy accommodates the nutritional demands of reproduction in a free‐living folivore, the Koala (Phascolarctos cinereus) , 2007 .

[16]  T. Dawson,et al.  Fiber Digestion in the Emu, Dromaius novaehollandiae, a Large Bird with a Simple Gut and High Rates of Passage , 1984, Physiological Zoology.

[17]  Z. J. Penefsky The determinants of contractility in the heart. , 1994, Comparative biochemistry and physiology. Physiology.

[18]  P.-E. Digestibility of krill ( Euphausia superba and Thysanoessa sp . ) in minke whales ( Balaenoptera acutorostrata ) and crabeater seals ( Lobodon carcinophagus ) " , 2005 .

[19]  Renaud Escudié,et al.  Total solids content drives high solid anaerobic digestion via mass transfer limitation. , 2012, Bioresource technology.

[20]  E. Sakaguchi,et al.  Fibre digestion and digesta retention time in guinea-pigs (Cavia porcellus), degus (Octodon degus) and leaf-eared mice (Phyllotis darwini). , 1992, Comparative biochemistry and physiology. Comparative physiology.

[21]  W. Gehring,et al.  Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Kühl,et al.  pH profiles of the extremely alkaline hindguts of soil-feeding termites (Isoptera: Termitidae) determined with microelectrodes , 1996 .

[23]  B. Sheffy,et al.  Sites of organic acid production and patterns of digesta movement in the gastrointestinal tract of dogs. , 1979, The Journal of nutrition.

[24]  I. Hume,et al.  Digestion and Digesta Passage in the Brushtail Possum, Trichosurus Vulpecula (Kerr). , 1981 .

[25]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[26]  Zhongtang Yu,et al.  Status of the phylogenetic diversity census of ruminal microbiomes. , 2011, FEMS microbiology ecology.

[27]  M. Clauss,et al.  The digestive performance of mammalian herbivores: why big may not be that much better , 2005 .

[28]  Angela Schwarm,et al.  A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[29]  E. Sakaguchi,et al.  Comparison of fibre digestion and digesta retention time between rabbits, guinea-pigs, rats and hamsters , 1987, British Journal of Nutrition.

[30]  P. Barboza Digestive Strategies of the Wombats: Feed Intake, Fiber Digestion, and Digesta Passage in Two Grazing Marsupials with Hindgut Fermentation , 1993, Physiological Zoology.

[31]  C. Stevens,et al.  Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. , 1998, Physiological reviews.

[32]  Carolyn D. Berdanier,et al.  Handbook of Nutrition and Food , 2001 .

[33]  Kate E. Jones,et al.  The delayed rise of present-day mammals , 1990, Nature.

[34]  O. Levenspiel Chemical Reaction Engineering , 1972 .

[35]  D. Mann,et al.  The nutrition of herbivores. , 1989 .

[36]  R. Knight,et al.  Worlds within worlds: evolution of the vertebrate gut microbiota , 2008, Nature Reviews Microbiology.

[37]  E. Zoetendal,et al.  Temperature Gradient Gel Electrophoresis Analysis of 16S rRNA from Human Fecal Samples Reveals Stable and Host-Specific Communities of Active Bacteria , 1998, Applied and Environmental Microbiology.

[38]  D. Wingate Comparative physiology of the vertebrate digestive system , 1989 .

[39]  Jacques Monod,et al.  LA TECHNIQUE DE CULTURE CONTINUE THÉORIE ET APPLICATIONS , 1978 .

[40]  A. Brauman Effect of gut transit and mound deposit on soil organic matter transformations in the soil feeding termite: a review. , 2000 .

[41]  E. Trably,et al.  Lignocellulosic Materials Into Biohydrogen and Biomethane: Impact of Structural Features and Pretreatment , 2013 .

[42]  Andreas Brune,et al.  Termite guts: the world's smallest bioreactors , 1998 .

[43]  E. Sakaguchi,et al.  Digesta retention and fibre digestion in brushtail possums, ringtail possums and rabbits. , 1990, Comparative biochemistry and physiology. A, Comparative physiology.

[44]  A. Kriete,et al.  Quantitative investigation of the area and volume in different compartments of the intestine of 18 mammalian species , 1991 .

[45]  E. Sakaguchi Digestive strategies of small hindgut fermenters , 2003 .

[46]  C. Angel A review of ratite nutrition , 1996 .

[47]  J. Ban The evolution of agriculture. , 1987 .

[48]  Hu Jinchu,et al.  The Giant Pandas of Wolong , 1985 .

[49]  P. Bork,et al.  A human gut microbial gene catalogue established by metagenomic sequencing , 2010, Nature.

[50]  G. Walsberg,et al.  Developmental and acclimatory contributions to water loss in a desert rodent: investigating the time course of adaptive change , 2001, Journal of Comparative Physiology B.

[51]  A. D. Thomas,et al.  Comparative anatomy and phylogenetic distribution of the mammalian cecal appendix , 2009, Journal of evolutionary biology.

[52]  K. Kock Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, Part I , 2005, Polar Biology.

[53]  P. Weimer,et al.  Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. , 2009, Bioresource technology.

[54]  A. Vogler,et al.  A comprehensive phylogenetic analysis of termites (Isoptera) illuminates key aspects of their evolutionary biology. , 2007, Molecular phylogenetics and evolution.

[55]  C. Stevens,et al.  Sites of organic acid production and pattern of digesta movement in the gastrointestinal tract of swine. , 1975, The Journal of nutrition.

[56]  P. Ehrlich,et al.  Introduction to insect biology and diversity , 1978 .

[57]  B. Hölldobler,et al.  Colony founding in Myrmecocystus mimicus wheeler (Hymenoptera: Formicidae) and the evolution of foundress associations , 1982, Behavioral Ecology and Sociobiology.

[58]  L. Cauquil,et al.  Potential core species and satellite species in the bacterial community within the rabbit caecum , 2008, FEMS microbiology ecology.

[59]  K. McCoy,et al.  Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. , 2007, Seminars in immunology.

[60]  A. Novick,et al.  Description of the chemostat. , 1950, Science.

[61]  J. Monod,et al.  Technique, Theory and Applications of Continuous Culture. , 1950 .

[62]  E. Sakaguchi,et al.  Fibre digestion and digesta retention from different physical forms of the feed in the rabbit. , 1992, Comparative biochemistry and physiology. Comparative physiology.

[63]  Roderick V. Jensen,et al.  Characterization of the fecal bacteria communities of forage-fed horses by pyrosequencing of 16S rRNA V4 gene amplicons. , 2012, FEMS microbiology letters.

[64]  D. Boucias,et al.  Multiple Levels of Synergistic Collaboration in Termite Lignocellulose Digestion , 2011, PloS one.

[65]  J. Doré,et al.  Direct Analysis of Genes Encoding 16S rRNA from Complex Communities Reveals Many Novel Molecular Species within the Human Gut , 1999, Applied and Environmental Microbiology.

[66]  C. Stevens,et al.  A comparison of gastrointestinal transit time in ten species of mammal , 1980, The Journal of Agricultural Science.

[67]  K. Nelson,et al.  The Microbial Community in the Feces of the Giant Panda (Ailuropoda melanoleuca) as Determined by PCR-TGGE Profiling and Clone Library Analysis , 2007, Microbial Ecology.

[68]  G. Wiggans,et al.  The measurement of liquid and solid digesta retention in ruminants, equines and rabbits given timothy (Phleum pratense) hay , 1982, British Journal of Nutrition.

[69]  Hongyu Zhang,et al.  The scarab gut: A potential bioreactor for bio‐fuel production , 2010 .

[70]  Todd J. McWhorter,et al.  Does Gut Function Limit Hummingbird Food Intake? , 2000, Physiological and Biochemical Zoology.

[71]  W. Engelhardt,et al.  Retention of digesta in the gastrointestinal tract of the guinea pig , 1986 .

[72]  Serge R. Guiot,et al.  Animal digestive strategies versus anaerobic digestion bioprocesses for biogas production from lignocellulosic biomass , 2011 .

[73]  J. Monod,et al.  Thetechnique of continuous culture. , 1950 .

[74]  T. Kudo,et al.  Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). , 2003, FEMS microbiology ecology.

[75]  Robert P Freckleton,et al.  Bergmann’s Rule and Body Size in Mammals , 2003, The American Naturalist.

[76]  D. Dellow Studies on the Nutrition of Macropodine Marsupials. 3. The Flow of Digesta Through the Stomach and Intestine of Macropodines and Sheep. , 1982 .

[77]  I. Hume,et al.  Effects of exercise and level of dietary protein on digestive function in horses. , 1985, Equine veterinary journal.

[78]  C. Dardillat,et al.  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 , 1993 .

[79]  U. Mueller,et al.  Free-living fungal symbionts (Lepiotaceae) of fungus-growing ants (Attini: Formicidae) , 2009, Mycologia.

[80]  H. Hirakawa Coprophagy in leporids and other mammalian herbivores , 2001 .