Molecular approach to the chemical characterization of fish-exuded kairomone: a Fourier transform infrared spectroscopic study

Abstract

Diel vertical migration (DVM) bioassay-guided Fourier transform infrared spectroscopy can be a prominent non-destructive and innovative approach for ecological studies. During the characterization of the nature of the fish-exuded kairomone, the peak area results from the spectroscopic analysis of the control, fish-conditioned (F) and temperature incubated fish-conditioned (IF) treatments of the DVM bioassays demonstrated that there was a strong correlation between the alterations of the amine N–H, amide II, amide IV and CH3 asymmetric vibrations, suggesting that both N–H and CH3 molecules may be main components of the fish-exuded kairomone cocktail. The IF treatment, which showed similar results with the control treatment, supported that the kairomone is inactivated by bacterial biodegradation. The seasonal variations in the peak areas of the N–H and CH3 bands suggested that DVM response varied seasonally, where migration response developed quickly in warmer seasons. The peak area of the amine N–H band of the F and IF treatments relative to control conditions can be used as an ideal indicator of the absence or presence and the promptness of migration, at all seasons.

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References

  1. Arrondo JLR, Muga A, Castresana J, Goñi FM (1993) Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy. Prog Biophys Mol Biol 59:23–56

    Article  CAS  PubMed  Google Scholar 

  2. Beklioglu M, Tan CO (2008) Drought complicated restoration of a Mediterranean shallow lake by biomanipulation. Fund Appl Limnol/Arch Hydrobiol 171:105–118

    Article  CAS  Google Scholar 

  3. Beklioglu M, Ince O, Tuzun I (2003) Restoration of eutrophic Lake Eymir, Turkey, by biomanipulation undertaken following a major external nutrient control I. Hydrobiologia 489:93–105

    Article  Google Scholar 

  4. Beklioglu M, Cetin AG, Zorlu P, Ay-Zog D (2006a) Role of planktonic bacteria in biodegradation of fish-exuded kairomone in laboratory bioassays of diel vertical migration. Arch Hydrobiol 165:89–104

    Article  Google Scholar 

  5. Beklioglu M, Telli M, Cetin AG (2006b) Fish and mucus-dwelling bacteria interact to produce a kairomone that induces diel vertical migration in Daphnia. Freshw Biol 51:2200–2206

    Article  Google Scholar 

  6. Boriss H, Boersma M, Wiltshire KH (1999) Trimethylamine induces migration of water fleas. Nature 398:382

    Article  CAS  Google Scholar 

  7. Bozkurt O, Bilgin MD, Severcan F (2007) The effect of diabetes mellitus on rat skeletal extensor digitorum longus muscle tissue: an FTIR study. Spectroscopy 21:151–160

    CAS  Google Scholar 

  8. Cakmak G, Togan I, Uguz C, Severcan F (2003) FT-IR spectroscopic analysis of rainbow trout liver exposed to nonylphenol. Appl Spectrosc 57:835–841

    Article  CAS  PubMed  Google Scholar 

  9. Cakmak G, Togan I, Severcan F (2006) 17β-Estradiol induced compositional, structural and functional changes in rainbow trout liver, revealed by FT-IR spectroscopy: a comparative study with nonylphenol. Aquat Toxicol 77:53–63

    Article  CAS  PubMed  Google Scholar 

  10. Chang MC, Tanaka J (2002) FT-IR study for hydroxyapatite/collagen nanocomposite cross-linked by glutaraldehyde. Biomaterials 23:4811–4818

    Article  CAS  PubMed  Google Scholar 

  11. Cohen Pj, Ritz A (2003) Role of kairomones in feeding interactions between seahorses and mysids. J Mar Biol Assoc UK 83:633–638

    Article  Google Scholar 

  12. Dawidowicz P, Loose CJ (1992) Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol Oceanogr 37:1589–1595

    Google Scholar 

  13. Dicke M, Sabelis M (1988) Infochemical terminology: based on cost–benefit analysis rather than origin of compounds? Funct Ecol 2:131–139

    Article  Google Scholar 

  14. Dodson SI (1988) The ecological role of chemical stimuli for the zooplankton: predator avoidance behavior in Daphnia. Limnol Oceanogr 33:1431–1439

    Google Scholar 

  15. Dogan A, Siyakus G, Severcan F (2006) FTIR spectroscopic characterization of irradiated hazelnut (Corylus avellana L.). Food Chem 100:1106–1114

    Article  CAS  Google Scholar 

  16. Forward RB Jr, Rittschof D (1999) Brine shrimp larval photoresponses involved in diel vertical migration: activation by fish mucus and modified amino sugars. Limnol Oceanogr 44:1904–1916

    CAS  Article  Google Scholar 

  17. Forward RB Jr, Rittschof D (2000) Alteration of photoresponses involved in diel vertical migration of a crab larva by fish mucus and degradation products of mucopolysaccharides. J Exp Mar Biol Ecol 245:277–292

    Article  CAS  PubMed  Google Scholar 

  18. Freifelder D (1982) Physical biochemistry: applications of biochemistry and molecular biology. W. H. Freeman and Co, New York

    Google Scholar 

  19. Garip S, Bozoglu F, Severcan F (2007) Differentiation of mesophilic and thermophilic bacteria with FTIR spectroscopy. Appl Spectrosc 61:186–192

    Article  CAS  PubMed  Google Scholar 

  20. Giordano M, Kansiz M, Heraud P, Beardall J, Wood B, McNaughton D (2001) Fourier transform infrared spectroscopy as a novel tool to investigate changes in intracellular macromolecular pools in the marine microalga Chaetoceros muellerii (Bacillariophyceae). J Phycol 37:271–279

    Article  CAS  Google Scholar 

  21. Gorgulu ST, Dogan M, Severcan F (2007) The characterization and differentiation of higher plants by Fourier transform infrared spectroscopy. Appl Spectrosc 61:300–308

    Article  CAS  PubMed  Google Scholar 

  22. Haris PI, Severcan F (1999) FTIR spectroscopic characterization of protein structure in aqueous and non-aqueous media. J Mol Catal B Enzym 7:207–221

    Article  CAS  Google Scholar 

  23. Hirschmugl CJ, Bayarri ZE, Bunta M, Holt JB, Giordano M (2006) Analysis of the nutritional status of algae by Fourier transform infrared chemical imaging. Infrared Phys Technol 49:57–63

    Article  CAS  Google Scholar 

  24. Jung C (2000) Insight into protein structure and protein–ligand recognition by Fourier transform infrared spectroscopy. J Mol Recognit 13:325–351

    Article  CAS  PubMed  Google Scholar 

  25. Kačuráková M, Wilson RH (2001) Developments in mid-infrared FT-IR spectroscopy of selected carbohydrates. Carbohydr Polym 44:291–303

    Article  Google Scholar 

  26. Lass S, Spaak P (2003a) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491:221–239

    Article  Google Scholar 

  27. Lass S, Spaak P (2003b) Temperature effects on chemical signaling in a predator–prey system. Freshw Biol 48:669–677

    Article  CAS  Google Scholar 

  28. Loose CJ, Dawidowicz P (1994) Trade-offs in diel vertical migration by zooplankton: the costs of predator avoidance. Ecology 75:2255–2263

    Article  Google Scholar 

  29. Loose CJ, von Elert E, Dawidowicz P (1993) Chemically-induced diel vertical migration in Daphnia—a new bioassay for kairomones exuded by fish. Arch Hydrobiol 126:329–337

    Google Scholar 

  30. Lürling M, Roozen F, van Donk E, Goser B (2003) Response of Daphnia to substances released from crowded congeners and conspecifics. J Plankton Res 25:967–978

    Article  Google Scholar 

  31. Maquelin K, Kirschner C, Choo-Smith LP, van den Braak N, Endtz HP, Naumann D, Puppels GJ (2002) Identification of medically relevant microorganisms by vibrational spectroscopy. J Microbiol Methods 51:255–271

    Article  CAS  PubMed  Google Scholar 

  32. McKelvey LM (1997) Planktivore chemical cues mediate zooplankton diel vertical migration. Ph.D. dissertation, Duke University

  33. Muluk CB, Beklioglu M (2005) Absence of typical diel vertical migration in Daphnia: varying role of water clarity, food, and dissolved oxygen in Lake Eymir, Turkey. Hydrobiologia 537:139–149

    Article  Google Scholar 

  34. Palaniappan PLRM, Vijayasundaram V (2008) Fourier transform infrared study of protein secondary structural changes in the muscle of Labeo rohita due to arsenic intoxication. Food Chem Toxicol 46:3534–3539

    Article  CAS  PubMed  Google Scholar 

  35. Palaniappan PLRM, Krishnakumar N, Vadivelu M (2008) FT-IR study of the effect of lead and the influence of chelating agents, DMSA and D-Penicillamine, on the biochemical contents of brain tissues of Catla catla fingerlings. Aquat Sci 70:314–322

    Article  CAS  Google Scholar 

  36. Parejko K, Dodson S (1990) Progress towards characterization of a predator/prey kairomone: Daphnia pulex and Chaoborus americanus. Hydrobiologia 198:51–59

    Article  Google Scholar 

  37. Pohnert G, von Elert E (2000) No ecological relevance of trimethylamine in fish-Daphnia interactions. Limnol Oceanogr 45:1153–1156

    CAS  Article  Google Scholar 

  38. Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204

    Article  PubMed  Google Scholar 

  39. Reede T (1995) Life history shifts in response to different levels of fish kairomones in Daphnia. J Plankton Res 17:1661–1667

    Article  Google Scholar 

  40. Ringelberg J, van Gool E (1998) Do bacteria, not fish, produce ‘fish kairomone’? J Plankton Res 20:1847–1852

    Article  Google Scholar 

  41. Rittschof D, Cohen JH (2004) Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25:1503–1516

    Article  CAS  PubMed  Google Scholar 

  42. Sakwinska O (2000) Trimethylamine does not trigger antipredatory life history shifts in Daphnia. Limnol Oceanogr 45:988–990

    Article  Google Scholar 

  43. Simsek Ozek N, Sara Y, Onur R, Severcan F (2009) Low dose simvastatin induces compositional, structural and dynamical changes on rat skeletal extensor digitorum longus muscle tissue. Biosci Rep (in press). doi:10.1042/BSR20080150

  44. Stehfest K, Toepel J, Wilhelm C (2005) The application of micro-FTIR spectroscopy to analyze nutrient stress-related changes in biomass composition of phytoplankton algae. Plant Physiol Biochem 43:717–726

    Article  CAS  PubMed  Google Scholar 

  45. Stibor H (1992) Predator-induced life-history shifts in a freshwater cladoceran. Oecologia 92:162–165

    Article  Google Scholar 

  46. Stibor H, Lampert W (2000) Components of additive variance in life-history traits of Daphnia hyalina: seasonal differences in the response to predator signals. Oikos 88:129–138

    Article  Google Scholar 

  47. Stuart B (1997) Biological applications of infrared spectroscopy. Wiley, Chichester

    Google Scholar 

  48. Tollrian R (1994) Fish–kairomone induced morphological changes in Daphnia lumholtzi (Sars). Arch Hydrobiol 130:69–75

    Google Scholar 

  49. van Donk E (2007) Chemical information transfer in freshwater plankton. Ecol Inform 2:112–120

    Article  Google Scholar 

  50. van Gool E, Ringelberg J (2002) Relationship between fish kairomone concentration in a lake and phototactic swimming by Daphnia. J Plankton Res 24:713–721

    Article  Google Scholar 

  51. van Holthoon FL, van Beek TA, Lürling M, Van Donk E, De Groot A (2003) Colony formation in Scenedesmus: a literature overview and further steps towards the chemical characterization of the Daphnia kairomone. Hydrobiologia 491:241–254

    Article  Google Scholar 

  52. von Elert E, Loose CJ (1996) Predator-induced diel vertical migration in Daphnia—enrichment and preliminary chemical characterization of a kairomone exuded by fish. J Chem Ecol 22:885–895

    Article  Google Scholar 

  53. von Elert E, Pohnert G (2000) Predator specificity of kairomones in diel vertical migration of Daphnia: a chemical approach. Oikos 88:119–128

    Article  Google Scholar 

  54. von Elert E, Stibor H (2006) Predator-mediated life history shifts in Daphnia: enrichment and preliminary chemical characterisation of a kairomone exuded by fish. Arch Hydrobiol 167:21–35

    Article  CAS  Google Scholar 

  55. Yasumoto K, Nishigami A, Yasumoto M, Kasai F, Okada Y, Kusumi T, Ooi T (2005) Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Lett 46:4765–4767

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Environment, Atmosphere, Earth and Marine Sciences group (ÇAYDAG-100Y035) of the Scientific and Technical Research Council of Turkey (TÜBİTAK). The authors thank Pelin Zorlu for carrying out the migration experiments.

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Correspondence to Feride Severcan.

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Akkas, S.B., Kepenek, A.O., Beklioglu, M. et al. Molecular approach to the chemical characterization of fish-exuded kairomone: a Fourier transform infrared spectroscopic study. Aquat. Sci. 72, 71–83 (2010). https://doi.org/10.1007/s00027-009-0114-2

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Keywords

  • Fish kairomone
  • Diel vertical migration
  • Infrared spectroscopy
  • Seasonality
  • Bacterial biodegradation