Transcriptional response of Atlantic salmon families to Piscirickettsia salmonis infection highlights the relevance of the iron-deprivation defence system

Abstract

BackgroundPiscirickettsiosis or Salmonid Rickettsial Septicaemia (SRS) is a bacterial disease that has a major economic impact on the Chilean salmon farming industry. Despite the fact that Piscirickettsia salmonis has been recognized as a major fish pathogen for over 20 years, the molecular strategies underlying the fish response to infection and the bacterial mechanisms of pathogenesis are poorly understood. We analysed and compared the head kidney transcriptional response of Atlantic salmon (Salmo salar) families with different levels of susceptibility to P. salmonis infection in order to reveal mechanisms that might confer infection resistance.ResultsWe ranked forty full-sibling Atlantic salmon families according to accumulated mortality after a challenge with P. salmonis and selected the families with the lowest and highest cumulative mortalities for microarray gene expression analysis. A comparison of the response to P. salmonis infection between low and high susceptibility groups identified biological processes presumably involved in natural resistance to the pathogen. In particular, expression changes of genes linked to cellular iron depletion, as well as low iron content and bacterial load in the head kidney of fish from low susceptibility families, suggest that iron-deprivation is an innate immunity defence mechanism against P. salmonis. To complement these results, we predicted a set of iron acquisition genes from the P. salmonis genome. Identification of putative Fur boxes and expression of the genes under iron-depleted conditions revealed that most of these genes form part of the Fur regulon of P. salmonis.ConclusionsThis study revealed, for the first time, differences in the transcriptional response to P. salmonis infection among Atlantic salmon families with varied levels of susceptibility to the infection. These differences correlated with changes in the abundance of transcripts encoding proteins directly and indirectly involved in the immune response; changes that highlighted the role of nutritional immunity through iron deprivation in host defence mechanisms against P. salmonis. Additionally, we found that P. salmonis has several mechanisms for iron acquisition, suggesting that this bacterium can obtain iron from different sources, including ferric iron through capturing endogenous and exogenous siderophores and ferrous iron. Our results contribute to determining the underlying resistance mechanisms of Atlantic salmon to P. salmonis infection and to identifying future treatment strategies.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1716-9) contains supplementary material, which is available to authorized users.

Discovery and functional annotation of quantitative trait loci affecting resistance to sea lice in Atlantic salmon

“…Chromosome 18 does not contain any clear candidate genes, but from a literature search alone, the most plausible gene is probably heme binding protein 2 (HEBP2). Reducing iron availability has been suggested as a possible mechanism of resistance to sea lice (Fast et al 2007; Sutherland et al 2014) and Piscirickettsia salmonis (Pulgar et al 2015) in Atlantic salmon.…”

Complete genome sequence of Piscirickettsia salmonis LF-89 (ATCC VR-1361) a major pathogen of farmed salmonid fish

“…It is known that intracellular pathogens have evolved complex mechanisms of iron acquisition to compete successfully with the host for the metal. In a previous work we predicted a cluster of genes encoding all enzymes necessary for siderophore biosynthesis and transport (Pulgar et al, 2015). Siderophores have the potential to be modified in order to improve the delivery of antibiotics by using them as Trojan horses, a biotechnological approach that have been employed to counter bacterial antibiotic resistance (Gorska et al, 2014).…”

Physiological evidence that Piscirickettsia salmonis produces siderophores and uses iron from different sources

“…The present study did not assess the chemical nature of siderophores (hydroxamate or catecholate type), and consequently, further research is needed to clarify this point. However, homolog genes for the biosynthesis and transport of vibrioferrin, a siderophore, were predicted in P. salmonis through in silico analyses of the previously obtained complete LF‐89 T genome (Pulgar, Hödar, et al., ; Pulgar, Travisany, et al., ) and partial P. salmonis AUSTRAL‐005 genome (Yañez et al., ). These analyses were conducted using a combined approach with the prediction programs Glimmer (Delcher, Bratke, Powers, & Salzberg, ), Artemis (Rutherford et al., ) and CD‐HIT (Fu, Niu, Zhu, Wu, & Li, ).…”