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Carbohydrate utilisation by microbial symbionts in the marine herbivorous fishes Odax cyanomelas and Crinodus lophodon


Carbohydrate uptake and catabolism by the gut microbiota of two species of temperate marine herbivorous fish were investigated using enzyme extracts prepared from microbial pellets. The fish studied were the herring cale Odax cyanomelas (Family Odacidae), which feeds on Ecklonia radiata, and the sea carp Crinodus lophodon (Family Aplodactylidae), which feeds primarily on red and green algae. Constitutive phosphoenolpyruvate phosphotransferase systems for glucose, galactose, fructose and mannitol were present in the microbiota of both fish. Hexokinase, fructokinase and mannitol dehydrogenase activities indicated that transport of the corresponding substrates may be coupled to permeases. Galactokinase activity was only detected in C. lophodon, as expected from its diet. Phosphofructokinase and pyruvate kinase activities were taken to indicate that carbohydrate metabolism proceeded via the fructose bisphosphate pathway. Differences in the transport and metabolism of the different monomers by the microbiota of O. cyanomelas and C. lophodon correlated strongly with predicted monomer availability in the gut of each species, suggesting that the microbiota are an integral component of digestion in these fish. The rates of production in adult fish of acetate, the major short-chain fatty acid, were estimated as 136 μmol·h-1 in O. cyanomelas and 166 μmol·h-1 in C. lophodon. These rates indicate that microbial fermentation is a potentially important source of energy for the host fish.

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AK :

acetate kinase


cetyl trimethylammonium bromide

FK :



fructose 1-phosphate

F1PK :

fructose 1-phosphate kinase

F1-6BP :

Fructose 1,6-bisphosphate

F6P :

fructose 6-phosphate

GK :


Gal1P :

galactose 1-phosphate

G6P :

glucose 6-phosphate

HK :



mannitol dehydrogenase

M1P :

mannitol 1-phosphate

M1-PDH :

mannitol 1-phosphate dehydrogenase





PK :

pyruvate kinase


phosphotransferase system


short-chain fatty acid(s)


trifluoroacetic acid


  1. Anderson RL, Sapico VL (1975) D-fructose (D-mannose) kinase. In: Wood WA (ed) Methods in enzymology, XLII. Academic Press, New York, pp 39–43

  2. Anderson TA (1991) Mechanisms of digestion in the marine herbivore, the luderick, Girella tricuspidata (Quoy and Gaimard). J Fish Biol 39:535–547

  3. Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85:57–68

  4. Andrews RW, King RM (1990) Selection of potentials for pulsed amperometric detection of carbohydrates at gold electrodes. Anal Chem 62:2130–2134

  5. Chappell DJ, Slaytor M (1993) Uric acid synthesis in freshly collected and laboratory-maintained Nasutitermes walkeri Hill. Insect Biochem Mol Biol 23:499–506

  6. Clements KD (1991) Gut microorganisms of surgeonfishes (Family Acanthuridae). Unpublished PhD thesis, James Cook University of North Queensland, Australia

  7. Clements KD, Gleeson VP, Slaytor M (1994) Short-chain fatty acid metabolism in temperature marine herbivorous fish. J Comp Physiol B 164:372–377

  8. Clements KD, Sutton DC, Choat JH (1989) Occurrence and characteristics of unusual protistan symbionts from surgeonfishes (Acanthuridae) of the Great Barrier Reef, Australia. Mar Biol 102:403–412

  9. Crans DC, Kazlauskas RJ, Hirschbein BL, Wong C, Abril O, Whitesides GM (1987) Enzymatic regeneration of adenosine 5′-triphosphate: acetyl phosphate, dihydroxyacetone phosphate, 5-phospho-α-D-ribosyl pyrophosphate, uridine-5′-diphosphoglucose. In: Mosbach K (ed) Methods in Enzymology, 136. Academic Press, New York, p 271

  10. Englyst HN, Hay S, Macfarlane GT (1987) Polysaccharide breakdown by mixed populations of human faecal bacteria. FEMS Microbiol Ecol 95:163–171

  11. Fengel D, Wegener G (1979) Hydrolysis of polysaccharides with trifluoroacetic acid and its application to rapid wool and pulp analysis. In Brown RD Jr, Jurasek L (eds) Hydrolysis of cellulose: mechanisms of enzymatic and acid catalysis, 181. Am Chem Soc, Washington, D.C., pp 145–158

  12. Fishelson L, Montgomery WL, Myrberg AA (1985) A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: Teleostei) from the Red Sea. Science 229:49–51

  13. Gleeson V (1992) Digestion in the marine herbivorous fish, Crinodus lophodon (Teleostei: Aplodactylidae), BSc (Hons) thesis, School of Biological Sciences, The University of Sydney

  14. Gottschalk G, Hugo HV (1982) Phosphofructokinase from Clostridium pasteurianum. In: Wood WA (ed) Methods in enzymology, 90. Academic Press, New York, pp 82–87

  15. Gottschalk G (1986) Bacterial metabolism, 2nd edn. Springer-Verlag, New York

  16. Heinrich MR, Howard SM (1966) Galactokinase. In: Wood WA (ed) Carbohydrate metabolism, IX. Academic Press, New York, pp 407–409

  17. Herbert D, Phipps PJ, Strange RE (1971) Chemical analysis of microbiol cells. In: Norris JR, Ribbons DW (eds) Methods in microbiology, 5B. Academic Press, London, pp 244–249

  18. Horecker BL (1966) Mannitol dehydrogenase (crystalline) from Lactobacillus brevis. In: Wood WA (ed) Methods in enzymology, IX. Academic Press, New York, p 143

  19. Horwitz SB (1966a) D-Mannitol 1-phosphate dehydrogenase and D-sorbitol 6-phosphate dehydrogenase from Aerobacter aerogenes. In: Wood WA (ed) Methods in enzymology, Academic Press, New York, IX. pp 150–152

  20. Horwitz SB (1966b) D-Mannitol 1-phosphate dehydrogenase and D-sorbitol dehydrogenase from Bacillus subtilis. In: Wood WA (ed) Methods in Enzymology, IX. Academic Press, New York, pp 155–156

  21. Kandel JS, Horn MH, Van Antwerp W (1994) Volatile fatty acids in the hindguts of herbivorous fishes from temperate and tropical marine waters. J Fish Biol 45:527–529

  22. Kornberg HL, Reeves RE (1972) Inducible phosphoenolpyruvate-dependent hexose phosphotransferase activities in Escherichia coli. Biochem J 128:1339–1344

  23. Kruger N (1989) Effects of temperature on the kinetic properties of phosphofructokinase from Escherichia coli. Trans Biochem Soc 17:760–761

  24. Lie YA, Stuetz RM, Madgwick JC (1990) Australian brown seaweeds as a source of polysaccharide and inorganic elements. Aust J Biotech 4:279–281

  25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 19:265–275

  26. Macfarlane GT, Englyst HN (1986) Starch utilisation by the human large intestinal microflora. J Appl Bacteriol 6:195–201

  27. Malcovati MM, Valentini G (1982) AMP- and fructose 1,6-bisphosphate-activated pyruvate kinases from Escherichia coli. In: Wood WA (ed) Methods in Enzymology, 90. Academic Press, New York, pp 170–179

  28. Martinez G, Barker HA, Horecker BL (1963) A specific mannitol dehydrogenase from Lactobacillus brevis. J Biol Chem 238:1598–1603

  29. Matchell WJ, Booth IR (1984) Characterisation of the Clostridium pasteurianum phosphotransferase system. J Gen Microbiol 130:2193–2200

  30. Mitchell WJ, Roohi MS, Mosely MJ, Booth IR (1987) Regulation of carbohydrate utilisation in clostridium pasteurianum J Gen Microbiol 133:31–36

  31. Moroshita Y, (1994) The effect of dietary mannitol on the caecal microflora and short-chain fatty acids in rats. Lett Appl Microbiol 18:27–29

  32. Mountfort DO, Grant WD, Morgan H, Rainey FA, Stackebrandt E (1993) Isolation and characterisation of an obligately anaerobic, pectinolytic member of the genus Eubacterium from mullet gut. Arch Microbiol 159:289–295

  33. Mountfort DO, Rainey FA, Burghardt J, Stackebrandt E (1994) Clostridium grantii sp. nov., a new obligately anaerobic, alginolytic bacterium isolated from mullet gut. Arch Microbiol 162:173–179

  34. Mountfort DO, Rhodes LL (1991) Anaerobic growth and fermentation characteristics of Paecilomyces lilacinus isolated from mullet gut. Appl Environ Microbiol 57:1963–1968

  35. Patni NJ, Alexander JK (1971) Utilization of glucose by Clostridium thermocellum: presence of glucokinase and other glycolytic enzymes in cell extracts. J Bacteriol 105:220–225

  36. Pereival E (1979) The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. Br Phycol J 14:103–117

  37. Percival E, McDowell RH (1967) Chemistry and enzymology of marine algal polysaccharides. Academic Press, London

  38. Prosser CL, Brown FA (1962) Comparative animal physiology, 2nd edn. Saunders, Philadelphia

  39. Rimmer DW (1986) Changes in diet and the development of microbial digestion in juvenile buffalo bream, Kyphosus cornelii. Mar Biol 92:443–448

  40. Rimmer DW, Wiebe WJ (1987) Fermentative microbial digestion in herbivorous fishes. J Fish Biol 31:229–236

  41. Russo MDF (1993) Digestive enzymes in two temperate marine herbivorous fish, Crinodus lophodon and Odax cyanomelas. BSc (Hons) thesis, Department of Biochemistry, The University of Sydney

  42. Saunders DR, Wiggins HS (1981) Conservation of mannitol, lactulose and raffinose by the human colon. Am J Physiol 241:G397-G402

  43. Schlegel HG, Zaborosch C (1993) General microbiology, 2nd edn. Cambridge University Press

  44. Titus E, Ahearn GA (1988) Short chain fatty acid transport in the intestine of a herbivorous teleost. J Exp Biol 135:77–94

  45. Titus E, Ahearn GA (1991) Transintestinal acetate transport in a herbivorous teleost: anion exchange at the basolateral membrane. J Exp Biol 156:41–61

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Correspondence to M. Slaytor.

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Communicated by I. D. Hume

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Seeto, G.S., Veivers, P.C., Clements, K.D. et al. Carbohydrate utilisation by microbial symbionts in the marine herbivorous fishes Odax cyanomelas and Crinodus lophodon . J Comp Physiol B 165, 571–579 (1996). https://doi.org/10.1007/BF00387519

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Key words

  • Temperate marine fish
  • Marine herbivorous fish
  • Carbohydrate fermentation
  • Herring cale, Odax cyanomelas
  • Sea carp, Crinodus lophodon