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Short-chain fatty acid metabolism in temperate marine herbivorous fish

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Abstract

Short-chain fatty acids (SCFAs) were identified and estimated in the gut of three herbivorous fish containing gut endosymbionts, the herring cale Odax cyanomelas (Richardson, 1850) (Family Odacidae), the butterfish O. pullus (Bloch and Schneider, 1801) (Family Odacidae) and the sea carp Crinodus lophodon (Günther, 1859) (Family Aplodactylidae). The highest concentrations of short-chain fatty acids were in the posterior region of the intestine in all species. In O. cyanomelas 85% of the total short-chain fatty acids were found in this region. There was a positive correlation between the distribution of short-chain fatty acids and the microorganisms, suggesting that the short-chain fatty acids were end products of microbial anaerobic metabolism. The major short-chain fatty acid in all three species was acetate, the concentration of which ranged from 20 to 29 mmol·1-1 in the posterior intestine. Lower concentrations of propionate and butyrate were also found. Additionally, valerate was found in the odacids. The ratio of acetate: propionate:butyrate:valerate in the gut section containing the highest concentration of short-chain fatty acids was 83:8:9:1 in O. cyanomelas, 64:21:14:1 in O. pullus and 74:17:9:0 in C. lophodon. Acetate was present in the blood of O. cyanomelas and C. lophodon at concentrations of 1.74±0.17 and 1.79±0.20 mmol·l-1, respectively. The presence of the enzyme necessary to activate acetate, acetyl CoA synthetase, in the major tissues of both O. cyanomelas and C. lophodon indicates that these fishes are able to utilise acetate produced in the gut. The highest activity of acetyl CoA synthetase, 3.55±0.51 and 6.48±3.18 nmol·s-1·g tissue-1 in O. cyanomelas and C. lophodon, respectively, was found in the kidney. Acetyl CoA hydrolase activity was detected in the liver, heart, muscle, gut and kidney of O. cyanomelas and C. lophodon. The highest activity was in the liver of both species, 91.22±9.03 and 57.35±7.15 nmol·s-1·g tissue-1 in O. cyanomelas and C. lophodon, respectively. The presence of acetyl CoA hydrolase in tissues of O. cyanomelas and C. lophodon raises the possibility that some of the acetate in the blood could arise from hydrolysis of endogenously produced acetyl CoA. The results strongly support the hypothesis that short-chain fatty acids produced by endosymbionts in the posterior intestine are used as a blood fuel either for energy purposes or for lipid synthesis by the host fish.

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Abbreviations

DTNB:

5,5-dithiobis [2-nitrobenzoic acid]

SCUBA:

self contained underwater breathing apparatus

SCFA:

short-chain fatty acid

TCA:

trichloroacetic acid

TRIS:

TRIS (hydroxymethyl) amino-methane

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Authors and Affiliations

  1. School of Biological Sciences, The University of Sydney, 2006, Sydney, N.S.W., Australia

    K. D. Clements & V. P. Gleeson

  2. Department of Biochemistry, The University of Sydney, 2006, Sydney, N.S.W., Australia

    M. Slaytor

Authors
  1. K. D. Clements
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  2. V. P. Gleeson
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  3. M. Slaytor
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Clements, K.D., Gleeson, V.P. & Slaytor, M. Short-chain fatty acid metabolism in temperate marine herbivorous fish. J Comp Physiol B 164, 372–377 (1994). https://doi.org/10.1007/BF00302552

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