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Identification, release and olfactory detection of bile salts in the intestinal fluid of the Senegalese sole (Solea senegalensis)

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Abstract

Olfactory sensitivity to bile salts is wide-spread in teleosts; however, which bile salts are released in sufficient quantities to be detected is unclear. The current study identified bile salts in the intestinal and bile fluids of Solea senegalensis by mass spectrometry–liquid chromatography and assessed their olfactory potency by the electro-olfactogram. The main bile salts identified in the bile were taurocholic acid (342 mM) and taurolithocholic acid (271 mM) plus a third, unidentified, bile salt of 532.3 Da. These three were also present in the intestinal fluid (taurocholic acid, 4.13 mM; taurolithocholic acid, 0.4 mM). In sole-conditioned water, only taurocholic acid (0.31 μM) was released in sufficient quantities to be measured (release rate: 24 nmol kg−1 min−1). Sole had high olfactory sensitivity to taurocholic acid but not to taurolithocholic acid. Furthermore, olfactory sensitivity was higher in the upper (right) olfactory epithelium than the lower (left). These two bile acids contribute about 40% of the olfactory potency of intestinal fluid and account for the difference in potency at the two epithelia. Taurocholic acid (but not taurolithocholic acid), and possibly other types of bile acid not tested, could be used as chemical signals and the upper olfactory epithelium is specialised for their detection.

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Abbreviations

EDTA:

Ethylene diamine tetra-acetic acid

EOG:

Electro-olfactogram

HPLC:

High-performance liquid chromatography

LC/MS:

Liquid chromatography/mass spectrometry

MS222:

3-Aminobenzoic acid ethyl ester

β-NAD+ :

β-Nicotinamide adenine dinucleotide

SEM:

Standard error of the mean

TCH:

Taurocholic acid

TLC:

Taurolithocholic acid

References

  • Agulleiro MJ, Anguis V, Cañavate JP, Martínez-Rodríguez G, Mylonas CC, Cerdà J (2006) Induction of spawning of captive-reared Senegal sole (Solea senegalensis) using different administration methods for gonadotropin-releasing hormone agonist. Aquaculture 257:511–524. doi:10.1016/j.aquaculture.2006.02.001

    Article  CAS  Google Scholar 

  • Anguis V, Cañavate JP (2005) Spawning of captive Senegal sole (Solea senegalensis) under a naturally fluctuating temperature regime. Aquaculture 243:133–145

    Article  Google Scholar 

  • Cabral HN (2000) Comparative feeding ecology of sympatric Solea solea and S. senegalensis, within nursery areas of the Tagus estuary, Portugal. J Fish Biol 57:1550–1562

    Article  Google Scholar 

  • Cabral H, Costa MJ (1999) Differential use of nursery areas within the Tagus estuary by sympatric soles, Solea solea and Solea senegalensis. Environ Biol Fishes 56:389–397

    Article  Google Scholar 

  • Døving KB, Selset R, Thommesen G (1980) Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol Scand 108:123–131

    Article  PubMed  Google Scholar 

  • Giaquinto PC, Hara TJ (2008) Discrimination of bile acids by the rainbow trout olfactory system: evidence as potential pheromones. Biol Res 41:33–42

    Article  PubMed  Google Scholar 

  • Goto T, Holzinger F, Hagey LR, Cerrè C, Ton-Nu H-T, Schteingart CD, Steinbach JH, Shneider BL, Hofmann AF (2003) Physicochemical and physiological properties of 5α-cyprinol sulfate, the toxic bile salt of cyprinid fish. J Lipid Res 44:1643–1651

    Article  PubMed  CAS  Google Scholar 

  • Hara TJ (1994a) The diversity of chemical stimulation in fish olfaction and gustation. Rev Fish Biol Fish 4:1–35

    Article  Google Scholar 

  • Hara TJ (1994b) Olfaction and gustation in fish: an overview. Acta Physiol Scand 152:207–217

    Article  PubMed  CAS  Google Scholar 

  • Haslewood GAD (1967) Bile salt evolution. J Lipid Res 8:535–550

    PubMed  CAS  Google Scholar 

  • Hofmann AF (1999) Bile acids: the good, the bad, and the ugly. News Physiol Sci 14:24–29

    PubMed  CAS  Google Scholar 

  • Hubbard PC, Barata EN, Canário AVM (2003) Olfactory sensitivity to catecholamines and their metabolites in the goldfish. Chem Senses 28:207–218

    Article  PubMed  CAS  Google Scholar 

  • Huertas M, Hubbard PC, Canário AM, Cerdà J (2007) Olfactory sensitivity to conspecific bile fluid and skin mucus in the European eel Anguilla anguilla (L). J Fish Biol 70:1907–1920

    Article  Google Scholar 

  • Iwata T, Yamasaki K (1964) Enzymatic determination and thin-layer chromatography of bile acids in blood. J Biochem 56:394–424

    Google Scholar 

  • Kasumyan AO (2004) The olfactory system in fish: structure, function, and role in behaviour. J Ichthyol 44(Suppl 2):S180–S223

    Google Scholar 

  • Kim S-K, Matsunari H, Takeuschi T, Yokoyama M, Murata Y, Ishihara K (2007) Effect of different dietary taurine levels on the conjugated bile acid composition and growth performance of juvenile and fingerling Japanese flounder Paralichthys olivaceus. Aquaculture 273:595–601. doi:10.1016/j.aquaculture.2007.10.031

    CAS  Google Scholar 

  • Li W, Scott AP, Siefkes MJ, Yan H, Liu Q, Yun S-S, Cage DA (2002) Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296:139–141

    Google Scholar 

  • Murphy GM, Biling BH, Baron DN (1970) A fluorimetric and enzymatic method for the estimation of serum total bile acids. J Clin Pathol 23:594–598

    Article  PubMed  CAS  Google Scholar 

  • Murphy GM, Maghsoudloo M, Qureshi MY (1995) Assay of bile acids in biological samples. In: Makin HLJ, Gower DB, Kirk DN (eds) Steroid analysis. Blackie Academic and Professional, Glasgow, pp 527–560

    Google Scholar 

  • Rodríguez-Gómez FJ, Rendón-Unceta C, Sarasquete C, Muñoz-Cueto JA (2001) Distribution of neuropeptide Y-like immunoreactivity in the brain of the Senegalese sole (Solea senegalensis). Anat Rec 262:227–237

    Article  PubMed  Google Scholar 

  • Sorensen PW, Caprio J (1998) Chemoreception. In: Evans DH (ed) The physiology of fishes, 2nd edn. CRC Press, Boca Raton, pp 375–405

    Google Scholar 

  • Sorensen PW, Fine JM, Dvornikovs V, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Hoye TR (2005) Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 1:324–328

    Article  PubMed  CAS  Google Scholar 

  • Une M, Goto T, Kihira K, Kuramoto T, Ki Hagiwara, Nakajima T, Hoshita T (1991) Isolation and identification of bile salts conjugated with cysteinolic acid from bile of the red seabream, Pagrosomus major. J Lipid Res 32:1619–1623

    PubMed  CAS  Google Scholar 

  • Velez Z, Hubbard PC, Barata EN, Canário AVM (2005) Evidence for functional asymmetry in the olfactory system of the Senegalese sole (Solea sensgalensis). Physiol Biochem Zool 78:756–765

    Article  PubMed  CAS  Google Scholar 

  • Velez Z, Hubbard PC, Barata EN, Canário AVM (2007a) Differential detection of conspecific-derived odorants by the two olfactory epithelia of the Senegalese sole (Solea senegalensis). Gen Comp Endocrinol 153:418–425. doi:10.1016/j.ygen.2007.02.016

    Article  PubMed  CAS  Google Scholar 

  • Velez Z, Hubbard PC, Hardege JD, Barata EN, Canário AVM (2007b) The contribution of amino acids to the odour of a prey species in the Senegalese sole (Solea senegalensis). Aquaculture 265:336–342. doi:10.1016/j.aquaculture.2007.02.029

    Article  CAS  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Pearson Higher Education, New Jersey

    Google Scholar 

  • Zhang C, Hara TJ (2009) Lake char (Salvelinus namaycush) olfactory neurons are highly sensitive and specific to bile acids. J Comp Physiol A 195:203–215. doi:10.1007/s00359-008-0399-y

    Article  CAS  Google Scholar 

  • Zhang C, Brown SB, Hara TJ (2001) Biochemical and physiological evidence that bile acids produced and released by lake char (Salvelinus namaycush) function as chemical signals. J Comp Physiol B 171:161–171. doi:10.1007/s003600000170

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was financed by grants SFRH/BD/16242/2004 and POCTI/CVT/38831/2001 from the Portuguese National Science Foundation and the European Union Social Funds for Regional Development. The authors wish to thank Drs. Neil Duncan, Joan Cerdà and Mar Huertas (Center of Aquaculture-IRTA, Tarragona, Spain) for collecting bile and intestinal fluids from sole. The experiments described herein comply with the “Principles of animal care” (No. 86-23, revised 1985) of the National Institute of Health (USA) and Portuguese national laws.

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Authors and Affiliations

  1. Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Zélia Velez, Peter C. Hubbard, Eduardo N. Barata & Adelino V. M. Canário

  2. Departamento de Biologia, Universidade de Évora, Evora, Portugal

    Zélia Velez & Eduardo N. Barata

  3. Department of Biological Sciences, University of Hull, Hull, UK

    Zélia Velez & Joerg D. Hardege

  4. Department of Chemistry, University of Hull, Hull, UK

    Kevin Welham

Authors
  1. Zélia Velez
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  2. Peter C. Hubbard
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  3. Kevin Welham
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  4. Joerg D. Hardege
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  5. Eduardo N. Barata
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  6. Adelino V. M. Canário
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Correspondence to Peter C. Hubbard.

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Velez, Z., Hubbard, P.C., Welham, K. et al. Identification, release and olfactory detection of bile salts in the intestinal fluid of the Senegalese sole (Solea senegalensis). J Comp Physiol A 195, 691–698 (2009). https://doi.org/10.1007/s00359-009-0444-5

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  • DOI: https://doi.org/10.1007/s00359-009-0444-5

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