Regular Article
Immunity to bacteria in fish

https://doi.org/10.1006/fsim.1998.0192Get rights and content

Abstract

Fish have many non-specific and specific, humoral and cellular mechanisms to resist bacterial diseases. Non-specific humoral factors include growth inhibiting substances, e.g. transferrin and antiproteases; lysins, e.g. lysozyme, C-reactive protein (CRP), bactericidal peptides and most importantly, complement which has lytic, proinflammatory, chemotactic and opsonic activities thus making a link with non-specific phagocyte responses. These are primarily executed by neutrophils and macrophages. The phagocytes contain many hydrolytic enzymes and when stimulated by bacteria produce reactive oxygen species (ROS), especially the hydroxyl radical, via generation of superoxide anions and nitric oxide. ROS are highly bactericidal. In addition, the neutrophils possess large quantities of myeloperoxidase (MPO) which generates bactericidal hypohalite ions from halide ions and H2O2. Macrophages can receive MPO from neutrophils and this may enhance their bactericidal activity. Antibody constitutes a specific humoral defence by inhibiting bacterial adherence or invasion of non-phagocytic host cells and neutralising bacterial toxins. Antibody can act as an opsonin and by activating complement by the classical pathway may lyse the bacterial cell, activate inflammation, phagocyte influx and further enhance phagocytosis. Macrophage bactericidal activity can be markedly increased by cytokines released by T lymphocytes on contact with their specific antigen. Pathogenic bacteria have evolved many ways of subverting these defence mechanisms of fish. These include the in vivo production of high affinity iron uptake systems (e.g. siderophores and their surface receptors, in Aeromonas salmonicida, Vibrio anguillarum). Some bacteria e.g. V. anguillarum strains of serotype 01, while being resistant to the alternative pathway of complement activation in normal serum, are killed in immune serum. In other bacteria, surface layers, capsules and elongated lipopolysaccharide (LPS) 0-antigens protect against classical complement-mediated killing (e.g. A. salmonicida, Photobacterium piscicida, V. anguillarum serotype 02 respectively). While some important pathogens (e.g. P. piscicida) are readily killed by macrophages, others (A. salmonicida) possess specialised superoxide dismutase and catalase to resist ROS and are toxic themselves to macrophages. Renibacterium salmoninarum uses antibody, complement and other serum components to activate the respiratory burst of macrophages on immediate contact thus exhausting this macrophage bactericidal mechanism before the bacterium is phagocytosed. Subsequently, R, salmoninarum is taken up by the macrophage where it multiplies as an intracellular pathogen. However, these two highly adapted pathogens, A. salmonicida and R. salmoninarum are both killed by activated macrophages indicating that the whole concerted efforts of specific and non-specific, humoral and cell-mediated immune responses are required for immunity against these two important pathogens.

References (87)

  • G.A. Davidson et al.

    Detection of specific and constitutive antibody secreting cells in the gills, head kidney and peripheral blood leucocytes of dab (Limanda limanda)

    Veterinary Immunology and Immunopathology

    (1997)
  • G.A. Davidson et al.

    Route of immunisation influences the generation of antibody secreting cells in the gut of rainbow trout (Oncorhynchus mykiss)

    Developmental and Comparative Immunology

    (1993)
  • A.E. Ellis

    Inhibition of the Aeromonas salmonicida extracellular protease by α2-macroglobulin in the serum of rainbow trout

    Microbial Pathogenesis

    (1987)
  • S.J. Freedman

    The role of α2-macroglobulin in furunculosis: a comparison of rainbow trout and brook trout

    Comparative Biochemistry and Physiology

    (1991)
  • J. Gercken et al.

    A new mannan-binding lectin from the serum of the eel (Anguilla anguilla L.): isolation, characterisation and comparison with the fucose-specific serum lectin

    Comparative Biochemistry and Physiology

    (1994)
  • B. Gudmundsdottir et al.

    Protection of Atlantic salmon (Salmo salar L.) against an experimental infection of Aeromonas salmonicida ssp.achromogenes

    Fish & Shellfish Immunology

    (1997)
  • L.J. Hardie et al.

    Effect of temperature on macrophage activation and the production of macrophage activating factor by rainbow trout (Oncorhynchus mykiss) leucocytes

    Developmental and Comparative Immunology

    (1994)
  • I.D. Hirst et al.

    Iron-regulated outer membrane proteins of Aeromonas salmonicida are important protective antigens in Atlantic salmon against furunculosis

    Fish & Shellfish Immunology

    (1994)
  • P.H.M. Joosten et al.

    Oral vaccination of fish against Vibrio anguillarum using alginate microparticles

    Fish & Shellfish Immunology

    (1997)
  • H. Kodama et al.

    Activation of trout macrophages and production of CRP after immunisation with Vibrio anguillarum

    Developmental and Comparative Immunology

    (1989)
  • P. Lazarovici et al.

    Purification and pore-forming activity of two hydrophobic polypeptides from the secretion of red sea moses sole, Pardachirus marmoratus)

    Journal of Biological Chemistry

    (1986)
  • J.S. Lumsden et al.

    Production of gill-associated and serum antibody by rainbow trout (Oncorhynchus mykiss) following immersion immunisation with acetone-killed Flavobacterium branchiophilum and the relationship to protection from experimental challenge

    Fish & Shellfish Immunology

    (1995)
  • B. Magariños et al.

    Influence of the capsular layer on the virulence of Pasturella piscicida for fish

    Microbial Pathogenesis

    ((1996))
  • B. Magariños et al.

    Adherence and invasive capacities of the fish pathogen Pasteurella piscicida

    FEMS Microbiology Letters

    (1996)
  • P.J. Midtlyng

    Vaccination against furunculosis

  • T. Murai et al.

    Isolation and characterisation of rainbow trout C-reactive protein

    Development and Comparative Immunology

    (1990)
  • M. Ohta et al.

    The mechanism of carbohydrate-mediated complement activation by the serum mannose-binding protein

    Journal of Biological Chemistry

    (1990)
  • G. Olivier et al.

    Interaction between Aeromonas salmonicida and peritoneal macrophages of brook trout (Salvelinus fontinalis)

    Veterinary Immunology and Immunopathology

    (1986)
  • J.H.W.M. Rombout et al.

    Differences in mucus and serum immunoglobulin of carp (Cyprinus carpio L.)

    Developmental and Comparative Immunology

    (1993)
  • C.J. Secombes

    The nonspecific immune system: cellular defences

  • C.J. Secombes et al.

    Host-pathogen interactions in salmonids

  • M.T. Silva et al.

    Neutrophil-macrophage cooperation in the host defence against mycobacterial infections

    Microbial Pathogenesis

    (1989)
  • A.J. Szalai et al.

    Changes in serum concentration of channel catfish (Ictalurus punctatus Rafinesque) phosphorylcholine – reactive protein (PRP) in response to inflammatory agents, low temperature shock and infection by the fungus Saprolegnia sp

    Fish & Shellfish Immunology

    (1994)
  • P.R. Waterstrat et al.

    In vitro responses of channel catfish, Ictalurus punctatus , neutrophils to Edwardsiella ictaluri

    Developmental and Comparative Immunology

    (1991)
  • A. White et al.

    Serum concentrations of C-reactive protein and serum amyloid P component in plaice (Pleuronectes platessa L.) in relation to season and injected lipopolysaccharide

    Comparative Biochemistry and Physiology

    (1983)
  • J.L. Winkelhake et al.

    Acute phase (C-reactive) protein-like macromolecules from rainbow trout (Salmo gairdneri)

    Developmental and Comparative Immunology

    (1982)
  • A.J. Ainsworth et al.

    Differences in the phagocytosis of four bacteria by channel catfish neutrophils

    Development and Comparative Immunology

    (1990)
  • G.J. Arason et al.

    An opsonin with mannan-binding protein (MBP)-like activity in the Atlantic salmon, Salmo salar

    Scandinavian Journal of Immunology

    (1994)
  • I. Bandin et al.

    Effect of serum factors on the survival of Renibacterium salmoninarum within rainbow trout macrophages

    Diseases of Aquatic Organisms

    (1995)
  • A.C. Barnes et al.

    Superoxide dismutase and catalase in Photobacterium damsela subsp piscicida and their roles in resistance to reactive oxygen species

    Microbiology

    ((1999))
  • Bernoth, E-M. Ellis, A. E. Midtlying, P. J. Olivier, G. Smith, P. 1997, Furunculosis: Multidisciplinary Fish Disease...
  • H.T. Boesen et al.

    Vibrio anguillarum resistance to rainbow trout (Oncorhynchus mykiss) serum: The role of lipopolysaccharide

    Infection and Immunity

    (1999)
  • R. Braun et al.

    Immunohistological localisation of trypsin in mucus-secreting layers of Atlantic salmon, Salmo salar L

    Journal of Fish Diseases

    (1990)
  • Cited by (499)

    View all citing articles on Scopus
    View full text