Skip to main content
Log in

Characterisation of l-alanine and glycine absorption across the gut of an ancient vertebrate

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

This study utilised an in vitro technique to characterise absorption of two amino acids across the intestinal epithelium of Pacific hagfish, Eptatretus stoutii. Uptake of l-alanine and glycine conformed to Michaelis–Menten kinetics. An uptake affinity (K m; substrate concentration required to attain a 50% uptake saturation) of 7.0 mM and an uptake capacity (J max) of 83 nmol cm−2 h−1 were described for l-alanine. The K m and J max for glycine were 2.2 mM and 11.9 nmol cm−2 h−1, respectively. Evidence suggested that the pathways of l-alanine and glycine absorption were shared, and sodium dependent. Further analysis indicated that glycine uptake was independent of luminal pH and proline, but a component of uptake was significantly impaired by 100-fold excesses of threonine or asparagine. The presence of a short-term (24 h) exposure to waterborne glycine, similar in nature to that which may be expected to occur when feeding inside an animal carcass, had no significant impact on gastrointestinal glycine uptake. This may indicate a lack of cross talk between absorptive epithelia. These results are the first published data to describe gastrointestinal uptake of an organic nutrient in the oldest extant vertebrate and may provide potential insight into the evolution of nutrient transport systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bakke AM, Glover CN, Krogdahl Ǻ (2011) Feeding, digestion and absorption of nutrients. In: Grosell M, Brauner CJ, Farrell AP (eds) The multifunctional gut of fish (fish physiology vol 30). Academic Press, London, pp 57–110

    Google Scholar 

  • Balocco C, Bogé G, Roche H (1993) Neutral amino-acid transport by marine fish intestine—role of the side-chain. J Comp Physiol B 163:340–347

    Article  CAS  Google Scholar 

  • Bardack D (1998) Relationships of living and fossil hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman and Hall, London, pp 3–14

    Google Scholar 

  • Barrington EJW (1945) The supposed pancreatic organs of Petromyzon fluviatilis and Myxine glutinosa. Q J Microsc Sci 340:391–417

    Google Scholar 

  • Bogé G, Roche H, Balocco C (2002) Amino acid transport by intestinal brush border vesicles of a marine fish, Boops salpa. Comp Biochem Physiol 131B:19–26

    Google Scholar 

  • Bröer S (2008) Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 88:249–286

    Article  PubMed  Google Scholar 

  • Bucking C, Glover CN, Wood CM (2011) Digestion under duress: nutrient acquisition and metabolism during hypoxia in hagfish (in submission)

  • Claiborne JB, Edwards SL, Morrison-Shetlar AI (2002) Acid–base regulation in fishes: cellular and molecular mechanisms. J Exp Zool 293:302–319

    Article  PubMed  CAS  Google Scholar 

  • Fänge R (1998) Hagfish blood cells and their formation. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman and Hall, London, pp 287–299

    Google Scholar 

  • Floge J, Stolte H, Kinne R (1984) Presence of a sodium-dependent d-glucose transport system in the kidney of the Atlantic hagfish (Myxine glutinosa). J Comp Physiol 154:355–364

    Google Scholar 

  • Forster ME (1990) Confirmation of the low metabolic rate of hagfish. Comp Biochem Physiol 96A:113–116

    Article  Google Scholar 

  • Forster ME, Fenwick JC (1994) Stimulation of calcium efflux from the hagfish, Eptatretus cirrhatus, gill pouch by an extract of corpuscles of Stannius from an eel (Anguilla dieffenbachia): Teleostei. Gen Comp Endocrinol 94:92–103

    Article  PubMed  CAS  Google Scholar 

  • Franklin NM, Glover CN, Nicol JA, Wood CM (2005) Calcium/cadmium interactions at uptake surfaces in rainbow trout: waterborne versus dietary routes of exposure. Environ Toxicol Chem 24:2954–2964

    Article  PubMed  CAS  Google Scholar 

  • Glover CN, Hogstrand C (2002) In vivo characterisation of intestinal zinc uptake in freshwater rainbow trout. J Exp Biol 205:141–150

    PubMed  CAS  Google Scholar 

  • Glover CN, Balesaria S, Mayer GD, Thompson ED, Walsh PJ, Hogstrand C (2003) Intestinal zinc uptake in two marine teleosts, squirrelfish (Holocentrus adscensionis) and Gulf toadfish (Opsanus beta). Physiol Biochem Zool 76:321–330

    Article  PubMed  CAS  Google Scholar 

  • Glover CN, Bucking C, Wood CM (2011) Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrate. Proc R Soc B (in press). doi:10.1098/rspb.2010.2784

  • Gundersen RY, Vaagnes P, Breivik T, Fonnum F, Opstad PK (2005) Glycine—an important neurotransmitter and cytoprotective agent. Acta Anaesthesiol Scand 49:1108–1116

    Article  PubMed  CAS  Google Scholar 

  • Karasov WH, Buddington RK, Diamond JM (1985) Adaptation of intestinal sugar and amino acid transport in vertebrate evolution. In: Gilles R, Gilles-Baillien M (eds) Transport processes, iono- and osmoregulation. Springer, Berlin, pp 227–239

    Google Scholar 

  • Martini FH (1998) The ecology of hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman and Hall, London, pp 57–78

    Google Scholar 

  • Nadella SR, Bucking C, Grosell M, Wood CM (2006a) Gastrointestinal assimilation of Cu during digestion of a single meal in the freshwater rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol 143:394–401

    Google Scholar 

  • Nadella SR, Grosell M, Wood CM (2006b) Physical characterization of high-affinity gastrointestinal Cu transport in vitro in freshwater rainbow trout Oncorhynchus mykiss. J Comp Physiol B 176:793–806

    Article  PubMed  CAS  Google Scholar 

  • Nilsson A, Fänge R (1970) Digestive proteases in the cyclostome Myxine glutinosa (L.). Comp Biochem Physiol 32:237–240

    Article  PubMed  CAS  Google Scholar 

  • Nilsson GE, Lutz PL (1991) Release of inhibitory neurotransmitters in response to anoxia in turtle brain. Am J Physiol 261:R32–R37

    PubMed  CAS  Google Scholar 

  • Secor SM, Diamond J (1995) Adaptive responses to feeding in Burmese pythons: pay before pumping. J Exp Biol 198:1313–1325

    PubMed  CAS  Google Scholar 

  • Storelli C, Verri T (1993) Nutrient transport in fish: studies with membrane vesicles. In: Lahlou B, Vitiello P (eds) Aquaculture: fundamental and applied research. American Geophysical Union, Washington, pp 139–157

    Google Scholar 

  • Sundberg BE, Wååg E, Jacobsson JA, Stephansson O, Rumaks J, Svirskis S, Alsiö J, Roman E, Ebendal T, Klusa V, Fredriksson R (2008) The evolutionary history and tissue mapping of amino acid transporters belonging to solute carrier families SLC32, SLC36, and SLC38. J Mol Neurosci 35:179–193

    Article  PubMed  CAS  Google Scholar 

  • Tamburri MN, Barry JP (1999) Adaptations for scavenging by three diverse bathyla species, Eptatretus stouti, Neptunea amianta and Orchomene obtusus. Deep-Sea Res I 46:2079–2093

    Article  Google Scholar 

  • Thorndyke MC, Falkmer SF (1998) The endocrine system of hagfishes. In: Jørgensen JM, Lomholt JP, Weber RE, Malte H (eds) The biology of hagfishes. Chapman and Hall, London, pp 399–412

    Google Scholar 

  • Uzzell T, Stolzenberg ED, Shinnar AE, Zasloff M (2003) Hagfish intestinal antimicrobial peptides are ancient cathelicidin. Peptides 24:1655–1667

    Article  PubMed  CAS  Google Scholar 

  • Vigna SR, Gorbman A (1979) Stimulation of intestinal lipase secretion by porcine cholecystokinin in the hagfish, Eptatretus stouti. Gen Comp Endocrinol 38:356–359

    Article  PubMed  CAS  Google Scholar 

  • Young JD, Yao SYM, Tse CM, Davies A, Baldwin SA (1994) Functional and molecular characteristics of a primitive vertebrate glucose transporter: studies of glucose transport by erythrocytes from the Pacific hagfish (Eptatretus stoutii). J Exp Biol 186:23–41

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Bruce Cameron (BMSC Research co-ordinator) and Dr. Sunita Nadella for excellent research support. Financial support was provided by an NSERC Discovery grant (CMW), and an NSERC Postdoctoral Fellowship (CB). CMW was also supported by the Canada Research Chair Program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chris N. Glover.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Glover, C.N., Bucking, C. & Wood, C.M. Characterisation of l-alanine and glycine absorption across the gut of an ancient vertebrate. J Comp Physiol B 181, 765–771 (2011). https://doi.org/10.1007/s00360-011-0571-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-011-0571-5

Keywords

Navigation