Skip to main content
SpringerLink
Log in

Hepatic mixed-function oxidases in California flatfishes are increased in contaminated environments and by oil and PCB ingestion

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Hepatic mixed-function oxidases (MFOs) were measured in the bothid flatfishes Citharicthys sordidus and C. stigmaeus from relatively uncontaminated and from polluted coastal populations of California, USA, at various times of the year during 1979–1980 and in individuals fed crude oil and polychlorinated biphenyl-augmented food in the laboratory. For C. sordidus, aryl hydrocarbon hydroxylase (AHH) specific activity was generally highest around the Los Angeles County sewage outfall on the Palos Verdes Shelf, intermediate near the 7-mile Hyperion sewage outfall in Santa Monica Bay and around a petroleum seep in the Santa Barbara Channel, and lowest in relatively unpolluted Monterey Bay. For C. stigmaeus, which had about ten times less specific activity than the foregoing species, specimens from the Santa Barbara petroleum seep had significantly greater AHH specific activity than those from Monterey Bay. Fishes from contaminated environments also showed increases of microsomal proteins with molecular weights of 56, 54, 57 and 46×103; moreover, the content of cytochrome P-450 was elevated in specimens of C. sordidus from such environments. Augmentation of food with seep oil or polychlorinated biphenyls (PCBs) induced significant increases in the specific activity of AHH and amounts of microsomal proteins in C. stigmaeus. Thus, these two species of flatfishes are good candidates for monitoring biologically meaningful levels of petroleum and polychlorinated biphenyls in contaminated environments. Moreover, the mixed function oxidase pattern in fish populations from the Santa Barbara petroleum seep is evidently a functional adaptation to chronic intake of petroleum hydrocarbons.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature Cited

  • Addison, R. F., M. E. Zinck and D. E. Willis: Mixed function oxidase enzymes in trout (Salvelinus fontinalis) liver: absence of induction following feeding of P,P-DDT or P,P′-DDE. Comp. Biochem. Physiol. 57C, 39–43 (1977)

    Google Scholar 

  • Ahokas, J., R. Paakkonen, K. Rönnholm, V. Raunnio, N. Kärki and O. Pelkonen: Oxidative metabolism of carcinogens by trout liver resulting in protein binding and mutagenicity. In: Microsomes and drug oxidations, pp 435–441. Ed. by V. Ullrich, I. Roots, A. Holdebrandt, R. W. Estabrook and A. H. Conney. Oxford: Pergamon Press 1977a

    Google Scholar 

  • Ahokas, J., O. Pelkonen and N. T. Kärki: Characterization of benzo(a)pyrene hydroxylase of trout liver. Cancer Res. 37, 3737–3743 (1977b)

    Google Scholar 

  • Ahokas, J., H. Saarni, D. W. Nebert and O. Pelkonen: The in vitro metabolism and covalent binding of benzo(a)pyrene to DNA catalyzed by trout liver microsomes. Chem. biol. Interactions 25, 103–111 (1979)

    Google Scholar 

  • Allen, A. A., R. S. Schlueter and P. G. Mikolaj: Natural oil seepage at Coal Oil Point, Santa Barbara, California. Science, N.Y. 170, 974–977 (1970)

    Google Scholar 

  • Allen, M. J.: Addition of Citharicthys fragilis Gilbert to the California fauna. Calif. Fish Game 62, 299–303 (1976)

    Google Scholar 

  • Bickers, D. R., A. Kappas and A. P. Alvares: Differences in inducibility of cutaneous and hepatic drug metabolizing enzymes and cytochrome P-450 by polychlorinated biphenyls and 1,1,1-trichloro-2,2-bis (p-chlorophenyl) ethane (DDT). J. Pharmac. exp. Ther. 188, 300–309 (1974)

    Google Scholar 

  • Boobis, A. R., D. W. Nebert and J. S. Felton: Comparison of B-napthoflavene and 3-methylcholanthrine as inducers of hepatic cytochrome(s) P-448 and aryl hydrocarbon [benzo(a)-pyrene] hydroxylase activity. Molec. Pharmac. 13, 259–263 (1977)

    Google Scholar 

  • Chambers, J. E. and J. D. Yarbrough: Xenobiotic biotransformation systems in fishes. Comp. Biochem. Physiol. 55C, 77–84 (1976)

    Google Scholar 

  • Chambers, J. E. and J. D. Yarbrough: A seasonal study of microsomal mixed function oxidase components in insecticide resistant and susceptible mosquito fish, Gambusia affinis. Toxicol. appl. Pharmac. 48, 497–507 (1979)

    Google Scholar 

  • DeWaide, J. H. and P. Th. Henderson: Seasonal variation of hepatic drug metabolism in the roach, Leusiscus rutilus, L. Comp. Biochem. Physiol. 32, 487–497 (1970)

    Google Scholar 

  • Gruger, E. H., Jr., M. M. Wekel, P. T. Numoto and D. R. Craddock: Induction of hepatic aryl hydrocarbon hydroxylase in salmon exposed to petroleum dissolved in seawater and to petroleum and polychlorinated biphenyls, separate and together, in food. Bull. envir. Contam. Toxicol. 17, 512–520 (1977)

    Google Scholar 

  • Haugen, D. A., M. J. Coon and D. W. Nebert: Induction of multiple forms of mouse liver cytochrome P-450. J. biol. Chem. 251, 1817–1827 (1976)

    Google Scholar 

  • Hill, D. W., E. Hejtmanick and B. J. Camp: Induction of hepatic microsomal enzymes by Aroclor® 1254 in Ictalurus punctatus (channel catfish). Bull. envir. Contam. Toxicol. 16, 495–501 (1976)

    Google Scholar 

  • James, M. D. and J. R. Bend: Polycyclic aromatic hydrocarbon induction of cytochrome P-450-dependent mixed-function oxidases in marine fish. Toxicol. appl. Pharmac. 54, 117–133 (1980)

    Google Scholar 

  • James, M. D., M. A. Q. Kahn and J. R. Bend: Hepatic mixed-function oxidase activities in several marine species common to coastal Florida. Comp. Biochem. Physiol. 62C, 155–164 (1979)

    Google Scholar 

  • Kurelec, B., S. Britvić, M. Rijavec, W. E. G. Müller and R. K. Zahn: Benzo(a)pyrene monooxygenase induction in marine fish — molecular response to oil pollution. Mar. Biol. 44, 211–216 (1977)

    Google Scholar 

  • Laemmli, U. K.: Cleavage of structural proteins during the assembly of the head of bacteriophage TH. Nature, Lond. 227, 680–685 (1970)

    Google Scholar 

  • Lee, R. F.: Mixed function oxidases in marine invertebrates. Mar. Biol. Lett. 2, 87–105 (1981)

    Google Scholar 

  • Lee, R. F., R. Sauerheber and G. H. Dobbs: Uptake, metabolism and discharge of polycyclic aromatic hydrocarbons by marine fish. Mar. Biol. 17, 201–208 (1972)

    Google Scholar 

  • Lowry, O. H., N. J. Rosebrough, A. L. Farr and R. J. Randall: Protein measurement with the folin phenol reagent. J. biol. Chem. 193, 265–275 (1951)

    Google Scholar 

  • McDermott, D. J. and T. C. Heesen: Inventory of DDT in sediments, Rep. sth. Calif. cstl Wat. Res. Proj. 4, 123–128 (1974)

    Google Scholar 

  • McDermott-Ehrlich, D., D. R. Young and T. C. Heesen: DDT and PCB in flatfish around southern California municipal outfalls. Chemosphere (U.K.), 7, 453–461 (1978)

    Google Scholar 

  • McGill, R., J. W. Tukey and W. A. Larsen: Variations of box plots. Am. Statistn 32, 12–16 (1978)

    Google Scholar 

  • Miller, D. J. and R. N. Lea: Guide to the coastal marine fishes of California, 235 pp. Sacramento, California: Department of Fish & Game 1972

    Google Scholar 

  • Nebert, D. W. and H. U. Gelboin: Substrate-inducible microsomal aryl hydrocarbon hydroxylase in mammalian cell culture. J. biol. Chem. 243, 6242–6249 (1968)

    Google Scholar 

  • Omura, T. and R. Sato: The carbon monoxide-binding pigment of liver microsomes. J. biol. Chem. 239, 2370–2378 (1964)

    Google Scholar 

  • Payne, J. F.: Field evaluation of benzopyrene hydroxylase induction as a monitor for marine petroleum pollution. Science, N.Y. 191, 945–946 (1976)

    Google Scholar 

  • Payne, J. F. and W. R. Penrose: Induction of aryl hydrocarbon [benzo(a)pyrenel hydroxylase in fish by petroleum. Bull. envir. Contam. Toxicol. 14, 112–116 (1975)

    Google Scholar 

  • Pederson, M. G., W. K. Hershberger, P. K. Zachariah and M. R. Juchau: Hepatic biotransformation of environmental xenobiotics in six strains of rainbow trout (Salmo gairdneri). J. Fish. Res. Bd Can. 33, 666–675 (1976)

    Google Scholar 

  • Philpot, R. M., M. O. James and J. R. Bend: Metabolism of benzo(a)pyrene and other xenobiotics by microsomal mixedfunction oxidases in marine species. In: Sources, effects and sinks of hydrocarbons in the aquatic environment, pp 184–199. Washington, D.C.: American Institute of Biological Sciences 1976

    Google Scholar 

  • Spies, R. B. and P. H. Davis: The infaunal benthos of a natural oil seep in the Santa Barbara Channel. Mar. Biol. 50, 227–237 (1979)

    Google Scholar 

  • Spies, R. B. and P. H. Davis: Toxicity of Santa Barbara seep oil to starfish embryos. III. Influence of parental exposure and the effects of other crude oils. Mar. envirl Res. 6, 3–11 (1982)

    Google Scholar 

  • Stegeman, J. J.: Influence of environmental contamination of cytochrome P-450 mixed-function oxygenases in fish: implications for recovery in the Wild Harbor Marsh. J. Fish. Res. Bd Can. 35, 668–674 (1978)

    Google Scholar 

  • Stegeman, J. J.: Mixed-function oxygenase studies in monitoring for effects of organic pollution. Rapp. P.-v. Réun. Cons. perm. int. Explor. Mer 179, 33–38 (1980)

    Google Scholar 

  • Stegeman, J. J.: Polynuclear aromatic hydrocarbons and their metabolism in the marine environment. In: Polycyclic hydrocarbons and cancer, Vol. 3. pp 1–60. Ed. by H. V. Gelboin and P. O. P. Ts'O. New York: Academic Press 1981

    Google Scholar 

  • Stegeman, J. J. and M. Chevion: Sex differences in cytochrome P-450 and mixed-function oxygenase activity in gonadallymature trout. Biochem. Pharmac. 29, 553–558 (1979)

    Google Scholar 

  • Stegeman, J. J., A. V. Klotz, B. R. Woodin and A. M. Pajor: Induction of hepatic cytochrome P-450 in fish and the indication of environmental induction in scup (Stenotomus chrysops). Aquat. Toxicol. 1, 197–212 (1981)

    Google Scholar 

  • Stegeman, J. J. and D. J. Sabo: Aspects of the effects of petroleum hydrocarbons on intermediary metabolism and xenobiotic metabolism in marine fish. In: Sources, effects and sinks of hydrocarbons in the aquatic environment, pp 423–436, Washington, D.C.: American Institute of Biological Sciences 1976

    Google Scholar 

  • Straughan, D.: Sublethal effects of natural chronic exposure to petroleum in the marine environment. Publs Am. Petrol. Inst. 4280, 1–120 (1976)

    Google Scholar 

  • Thomas, P. E., A. Y. H. Lu, D. Ryan, S. B. West, J. Kawalck and W. Levin: Immunochemical evidence for six forms of rat liver cytochrome P-450 obtained using antibodies against purified rat liver cytochromes P-450 and P-488. Molec. Pharmac. 12, 746–758 (1976)

    Google Scholar 

  • Varanasi, U. and D. J. Gmur: Metabolic activation and covalent binding of benzo(a)pyrene to deoxyribonucleic acid catalyzed by liver enzymes of marine fish. Biochem. Pharmac. 29, 753–761 (1980)

    Google Scholar 

  • Varanasi, U. and D. C. Malins: Metabolism of petroleum hydrocarbons: accumulation and biotransformation in marine organisms. In: Effects of petroleum on arctic and subarctic marine environments and organisms. Vol. II. Biological effects, pp 175–270. Ed. by D. C. Malins. New York: Academic Press 1977

    Google Scholar 

  • Walton, D. G., W. R. Penrose and J. M. Green: The petroleum-inducible mixed function oxidase of cunner (Tautogolabrus adspersus Walbaum 1792): some characteristics relevant to hydrocarbon monitoring. J. Fish. Res. Bd Can. 35, 1547–1552 (1978)

    Google Scholar 

  • Young, D. R. and T. C. Heesen: DDT, PCB and chlorinated benzenes in the marine ecosystem off southern California. In: Water chlorination: environmental impact and health effects, Vol. 2. pp 267–290. Ed. by R. L. Jolley, H. Corcher and D. H. Hamilton, Jr., Ann Arbor, Michigan: Ann Arbor Science Publishers 1978

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Lawrence Livermore National Laboratory, University of California, 94550, Livermore, California, USA

    R. B. Spies, J. S. Felton & L. Dillard

Authors
  1. R. B. Spies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. S. Felton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Dillard
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by N. D. Holland, La Jolla

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spies, R.B., Felton, J.S. & Dillard, L. Hepatic mixed-function oxidases in California flatfishes are increased in contaminated environments and by oil and PCB ingestion. Mar. Biol. 70, 117–127 (1982). https://doi.org/10.1007/BF00397675

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00397675

Keywords

Search

Navigation