High mortality of juvenile gilthead sea bream (Sparus aurata) from photobacteriosis is associated with alternative macrophage activation and anti-inflammatory response: Results of gene expression profiling of early responses in the head kidney

• Published in: Fish & shellfish immunology Vol. 34; no. 5; pp. 1269 - 1278
• Main Authors: Pellizzari, Caterina, Krasnov, Aleksei, Afanasyev, Sergey, Vitulo, Nicola, Franch, Rafaella, Pegolo, Sara, Patarnello, Tomaso, Bargelloni, Luca
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01-05-2013
• Subjects: Animals; Base Sequence; Fish Diseases - immunology; Fish Diseases - microbiology; Fish Diseases - mortality; Fish Proteins - genetics; Fish Proteins - metabolism; Gene Expression Profiling - veterinary; Gene Expression Regulation; Gram-Negative Bacterial Infections - immunology; Gram-Negative Bacterial Infections - microbiology; Gram-Negative Bacterial Infections - mortality; Gram-Negative Bacterial Infections - veterinary; Head kidney; Head Kidney - immunology; Head Kidney - metabolism; Head Kidney - microbiology; Immune suppression; Macrophage Activation; Molecular Sequence Data; Oligonucleotide Array Sequence Analysis - veterinary; Photobacteriosis; Photobacterium - immunology; Photobacterium - pathogenicity; Polymerase Chain Reaction - veterinary; Sea bream; Sea Bream - genetics; Sea Bream - metabolism; Sequence Homology; Transcriptomic analyses; Virulence; Transcriptomic analyses; Sea bream; Head kidney; Immune suppression; Photobacteriosis
• ISSN: 1050-4648; 1095-9947
• DOI: 10.1016/j.fsi.2013.02.007

The halophilic bacterium Photobacterium damselae subsp. piscicida (Phdp) represents a substantial health problem for several fish species in aquaculture. Bacteria that reside free and inside phagocytes cause acute and chronic forms of photobacteriosis. Infections of juveniles rapidly kill up to 90–100% fish. Factors underlying failure of the immune protection against bacteria remain largely unknown. The reported study used a transcriptomic approach to address this issue. Juvenile sea breams (0.5 g) were challenged by immersion in salt water containing 2.89 × 108 CFU of a virulent Phdp and the head kidney was sampled after 24- and 48-h. Analyses were performed using the second version of a 44 k oligonucleotide DNA microarray that represents 19,734 sea bream unique transcripts and covers diverse immune pathways. Expression changes of selected immune genes were validated with qPCR. Results suggested rapid recognition of the pathogen, as testified by up-regulation of lectins and antibacterial proteins (bactericidal permeability-increasing protein lectins, lysozyme, intracellular and extracellular proteases), chemokines and chemokine receptors. Increased expression of proteins involved in iron and heme metabolism also could be a response against bacteria that are dependent on iron. However, negative regulators of immune/inflammatory response were preponderant among the up-regulated genes. A remarkable finding was the increased expression of IL-10 in concert with up-regulation of arginase I and II and proteins of the polyamine biosynthesis pathway that diverts the arginine flux from the production of reactive nitrogen species. Such expression changes are characteristic for alternatively activated macrophages that do not develop acute inflammatory responses. Immune suppression can be induced by the host to reduce tissue damages or by the pathogen to evade host response.
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► Mechanisms for high susceptibility of sea bream to photobacteriosis were explored. ► Early responses were monitored by transcriptomic profiling of head kidney. ► Anti-inflammatory and cell-protective changes were mainly observed. ► Alternative macrophages activation pathway seemed to be favoured after infection.