Metabolomics

, Volume 1, Issue 2, pp 199–209 | Cite as

Characterizing the metabolic actions of natural stresses in the California red abalone, Haliotis rufescens using 1H NMR metabolomics

  • E. S. Rosenblum
  • M. R. Viant
  • B. M. Braid
  • J. D. Moore
  • C. S. Friedman
  • R. S. Tjeerdema
Article

Withering syndrome in California red abalone (Haliotis rufescens) is caused by the Rickettsiales-like prokaryote (WS-RLP) Candidatus Xenohaliotis californiensis. WS-RLP infection is not sufficient to cause withering syndrome, and for reasons not yet well understood additional stressors such as elevated water temperature appear to influence disease development. Using nuclear magnetic resonance (NMR) based metabolomics, we have investigated the influence of food availability, temperature, and bacterial infection, both individually and in combination, on the metabolic status of the red abalone. Food limitation caused dramatic reductions in all observed classes of foot muscle metabolites, while at the same time metabolite levels within the digestive gland were preserved or increased. We also found that food limitation in combination with elevated temperature led to greater metabolic perturbations in both tissue types than those observed under food limitation alone. WS-RLP infection and food-limitation resulted in many of the same metabolic changes within the tissues studied, although the effects of infection were less severe. We observed increased levels of homarine in the digestive gland of both food-limited and WS-RLP-infected animals, yet only observed increased homarine levels in the foot muscle of infected abalone. These results further support the recently established glucose-to-homarine ratio in foot muscle as a potential marker for differentiating WS-RLP-infected animals from those of both healthy and food limited abalone. Furthermore, we found that the NMR metabolic data correlates well with histological measurements supporting the use of the metabolomics approach for characterizing both normal and pathological events in marine species, particularly during periods of environmentally relevant stress.

Key words

withering syndrome abalone NMR metabolomics disease homarine 

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References

  1. Allen, W.V., Kilgore, J. 1975The essential amino acid requirements of the red abalone, Haliotis rufescensComp. Biochem. Physiol.50771775CrossRefGoogle Scholar
  2. Andree, K.B., Friedman, C.S., Moore, J.D., Hedrick, R.P. 2000A polymerase chain reaction assay for the detection of genomic DNA of a Rickettsiales-like prokaryote associated with withering syndrome in California abaloneJ. Shellfish Res.19213218Google Scholar
  3. Bayne, B.L.,  et al. 1985

    The effects of stress and pollution on marine animals

    Bayne, B.L.Brown, D.A.Burns, K. eds. Ecological Consequences of StressPraegerNew York141157
    Google Scholar
  4. Berking, S. 1987Homarine (n-methylpicolinic acid) and trigonelline (N-methylnicotinic acid) appear to be involved in pattern control in a marine hydroidDevelopment99211220PubMedGoogle Scholar
  5. Braid, B.A., Moore, J.D., Robbins, T.T., et al. (2004). Biochemical and histologic changes in red abalone (Haliotis rufescens) subjected to eight different treatment combinations of exposure to the agent of withering syndrome, water temperature, and food availability. MS Thesis, UC Davis, 1–98Google Scholar
  6. Brass, E.P., Hoppel, C.L. 1978Carnitinte metabolism in the fasting ratJ. Biol. Chem.25326882693PubMedGoogle Scholar
  7. Bremer, J. 1983Carnitinte Metabolism and functionsPhysiol. Rev.6314201480PubMedGoogle Scholar
  8. Carefoot, T.H. 1987Diet and its effect on oxygen uptake in the sea hare AplysiaJ. Exp. Mar. Biol. Ecol.114275287CrossRefGoogle Scholar
  9. Carefoot, T.H., Qian, P.Y., Taylor, B.E., West, T., Osborne, J. 1993The effects of starvation on energy reserves and metabolism in the northern abalone, Haliotis kamtschatkanaAquaculture118315325CrossRefGoogle Scholar
  10. Chiou, T., Lai, M., Shiau, C. 2001Seasonal variations of chemical constituents in the muscle and viscera of small abalone fed different dietsFish. Sci.67146156CrossRefGoogle Scholar
  11. Dall, W. 1975The role of ninhydrin-positive substances in osmoregulation in the western rock lobster, Panulirus longipesJ. Exp. Mar. Biol. Ecol.194358CrossRefGoogle Scholar
  12. Fan, T. 1996Metabolite profiling by one and two dimensional NMR analysis of complex mixturesProg. Nucl. Magn. Reson.28161219Google Scholar
  13. Friedman, C.S., Andree, K.B., Robbins, T.T.,  et al. 2000Candidatus Xenohaliotis californiensis,” a newly described bacterial pathogen and etiological agent of withering syndrome found in abalone Haliotis spp., along the west coast of North AmericaJ. Shellfish Res.19513Google Scholar
  14. Friedman, C.S., Finley, C.A. 2003Anthropogenic introduction of the etiological agent of withering syndrome into northern California abalone populations via conservation effortsCan. J. Fish. Aquat. Sci.6014241431CrossRefGoogle Scholar
  15. Friedman, C.S., Thomson, M., Chun, C.,  et al. 1997Withering syndrome of the black abalone Haliotis cracherodii (Leach): Water temperature, food availability, and parasites as possible causesJ. Shellfish Res.16403411Google Scholar
  16. Gardner, G.R., Harshbarger, J.C., Lake, J.,  et al. 1995Association of prokaryotes with symptomatic appearance of withering syndrome in black abalone Haliotis cracherodiiJ. Invertebr. Pathol.66111120CrossRefPubMedGoogle Scholar
  17. Gatty, G., Wilson, J.H. 1986Effect of body size starvation, temperature and oxygen tension on the oxygen consumption of hatchery reared ormers Haliotis tuberculata LAquaculture56229237CrossRefGoogle Scholar
  18. Hwang, D., Liang, W., Shiau, C., Chiou, T., Jeng, S. 1997Seasonal variations of free amino acids in the muscle and viscera of small abalone Haliotis diversicolorFish. Sci.63625629Google Scholar
  19. Hatae, K., Nakai, H., Shimada, A.,  et al. 1995Abalone (Haliotis discus): seasonal variations in chemical composition and textural propertiesJ. Food Sci.603235Google Scholar
  20. Isani, G., Serra, R., Cattani, O., Cortesi, P., Carpene, E. 1997Adenylaye energy charge and metallothionein as stress indices in Mytilus galloprovincialis exposed to cadmium and anoxiaJ. Mar. Biol. Assoc. UK7711871197Google Scholar
  21. Kasschau, M.R. 1975The relationship of free amino acids to salinity changes and temperature-salinity interactions in the mud flat snail, Nassarius obsoletusComp. Biochem. Physiol.51301308CrossRefGoogle Scholar
  22. Keller, M.D., Kiene, R.P., Matrai, P.A, Bellows, W.K. 1999Production of glycine betaine and dimethylsulfoniopropionate in marine phytoplankton. II. N-limited chemostat culturesMar. Biol.135249257CrossRefGoogle Scholar
  23. Kismohandaka, G., Friedman, C.S., Roberts, W., Hedrick, R.P., Crosby, M.P. 1993Investigation of physiological parameters of black abalone with withering syndromeJ. Shellfish Res.12131132Google Scholar
  24. Lafferty, K.D., Kuris, A.M. 1993Mass mortality of abalone Haliotis cracherodii in the California Channel Islands: tests of epidemiological hypothesesMar. Ecol. Prog. Ser.96 239248Google Scholar
  25. McCoid, M., Miget, R., Finne, G. 1984Effect of environmental salinity on the free amino acid compostion and concentration in penaeid shrimpJ. Food Sci.49327330Google Scholar
  26. Moore, J.D., Robbins, T.T., Friedman, C.S. 2000Withering syndrome in farmed red abalone, Haliotis rufescens: thermal induction and association with a gastrointestinal Rickettsiales-like prokaryoteJ. Aquat. Animal Health122634CrossRefGoogle Scholar
  27. Moore, J.D., Robbins, T.T., Hedrick, R.P., Friedman, C.S. 2001Transmission of the rickettsiales-like prokaryote Candidates Xenohalliotis californiensis and its role in withering syndrome of California abaloneJ. Shellfish Res.20867874Google Scholar
  28. Moore, J.D., Finley, C.A., Robbins, T.T., Friedman, C.S. 2002Withering syndrome and restoration of Southern California abalone populationsCalifornia Coop. Ocean. Fish. Invest. Rep.43112117Google Scholar
  29. Nelson, M.W., Leighton, D.L., Phleger, C.F., Nichols, P.D. 2002Comparsion of the growth and lipid compostion in the green abalone Haliotis fulgens, provided specific macroalgal dietsComp. Biochem. Physiol. Part B131695712CrossRefGoogle Scholar
  30. Netherton, J.C., Gurin, S. 1982Biosynthesis and physiological role of homarine in marine shrimpJ. Biol. Chem.2571197111975PubMedGoogle Scholar
  31. Okama, E., Abe, H. 1998Effects of starvation and D-or L-alanine administration on the free D- and L-alanine levels in the muscle and hepatopancrease of the crayfish Procambarus clarkiaComp. Biochem. Physiol. Part A120681686CrossRefGoogle Scholar
  32. Paul, A.J., Paul, J.M. 1998Respiration rate and thermal tolerances of pinto abalone Haliotis kamtschatkanaJ. Shellfish Res.17743745Google Scholar
  33. Pearson, D.J., Tubbs, P.K. 1967and derivatives in rat tissuesBiochem. J.105953963Google Scholar
  34. Rainbow, P.H., Phillips, D.J.H. 1993Cosmopolitan biomonitors of trace metalsMar. Poll. Bull.26593601CrossRefGoogle Scholar
  35. Raimondi, P.T., Wilson, C.M., Ambrose, R.F.,  et al. 2002Continued declines of black abalone along the coast of California: are mass mortalities related to El Nino events?Mar. Ecol. Prog. Ser.242143152Google Scholar
  36. Riley, R.T. 1976Changes in the total protein, lipid, carbohydrate, and extracellular body fluid free amino acids of the pacific oyster, Crassostrea gigas, during starvationProc. Nat. Shellfish Assoc.658490Google Scholar
  37. Schoffeniels, E. 1976Adaptation with respect to salinityBiochem. Soc. Symp.41179204PubMedGoogle Scholar
  38. Shields, J.D., Perkins, F.O., Friedman, C.S. 1996Hematological pathology of withering syndromeJ. Shellfish Res.15498Google Scholar
  39. Viant, M.R. 2003Improved methods for the acquisition and interpretation of NMR metabolomic dataBiochem. Biophys. Res. Comm.310943948CrossRefPubMedGoogle Scholar
  40. Viant, M.R, Rosenblum, E.S., Tjeerdema, R.T. 2003NMR-based metabolomics: a powerful approach for characterizing the effects of environmental stressors on organism healthEnviron. Sci. Technol.3749824989CrossRefPubMedGoogle Scholar
  41. Vilchis, L.I., Tegner, M.J., Moore, J.D., Friedman, C.S., et al. (2005). Effects of ocean warming on the growth, reproduction, and survivorship of red and green abalones in southern California: implications for restoration and recovery of depleted stocks. Ecol. Appl. 15, 469–480Google Scholar
  42. Voltzow, J. 1994

    Gastropoda: Prosobranchia

    Harrison, F.Humes, A. eds. Microscopic Anatomy of Invertebrates, Vol. 3Wiley-Liss PublishersNew York11252
    Google Scholar
  43. Von Brand, T., Nolan, M.O., Mann, E.R. 1948Observations on the respiration of Australorbis glabratus and some other aquatic snailsBiol. Bull. Woods Hole.95199213Google Scholar
  44. Watanabe, H., Yamanaka, H., Yamakawa, H. 1993Changes in the content of extractive components in disk abalone fed with marine algae and starvedNippon Suisan Gakk.5920312036Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  • E. S. Rosenblum
    • 1
  • M. R. Viant
    • 2
  • B. M. Braid
    • 3
  • J. D. Moore
    • 3
  • C. S. Friedman
    • 4
  • R. S. Tjeerdema
    • 1
  1. 1.Department of Environmental ToxicologyUniversity of CaliforniaDavisUSA
  2. 2.School of BiosciencesThe University of BirminghamEdgbaston, BirminghamUK
  3. 3.School of Veterinary MedicineUniversity of CaliforniaDavisUSA
  4. 4.School of Aquatic and Fishery SciencesUniversity of WashingtonSeattleUSA

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