Disease resistance in Atlantic salmon (Salmo salar): coinfection of the intracellular bacterial pathogen Piscirickettsia salmonis and the sea louse Caligus rogercresseyi

PLoS One. 2014 Apr 15;9(4):e95397. doi: 10.1371/journal.pone.0095397. eCollection 2014.

Abstract

Background: Naturally occurring coinfections of pathogens have been reported in salmonids, but their consequences on disease resistance are unclear. We hypothesized that 1) coinfection of Caligus rogercresseyi reduces the resistance of Atlantic salmon to Piscirickettsia salmonis; and 2) coinfection resistance is a heritable trait that does not correlate with resistance to a single infection.

Methodology: In total, 1,634 pedigreed Atlantic salmon were exposed to a single infection (SI) of P. salmonis (primary pathogen) or coinfection with C. rogercresseyi (secondary pathogen). Low and high level of coinfection were evaluated (LC = 44 copepodites per fish; HC = 88 copepodites per fish). Survival and quantitative genetic analyses were performed to determine the resistance to the single infection and coinfections.

Main findings: C. rogercresseyi significantly increased the mortality in fish infected with P. salmonis (SI mortality = 251/545; LC mortality = 544/544 and HC mortality = 545/545). Heritability estimates for resistance to P. salmonis were similar and of medium magnitude in all treatments (h2SI = 0.23 ± 0.07; h2LC = 0.17 ± 0.08; h2HC = 0.24 ± 0.07). A large and significant genetic correlation with regard to resistance was observed between coinfection treatments (rg LC-HC = 0.99 ± 0.01) but not between the single and coinfection treatments (rg SI-LC = -0.14 ± 0.33; rg SI-HC = 0.32 ± 0.34).

Conclusions/significance: C. rogercresseyi, as a secondary pathogen, reduces the resistance of Atlantic salmon to the pathogen P. salmonis. Resistance to coinfection of Piscirickettsia salmonis and Caligus rogercresseyi in Atlantic salmon is a heritable trait. The absence of a genetic correlation between resistance to a single infection and resistance to coinfection indicates that different genes control these processes. Coinfection of different pathogens and resistance to coinfection needs to be considered in future research on salmon farming, selective breeding and conservation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Coinfection / genetics
  • Coinfection / immunology*
  • Copepoda / physiology*
  • Disease Resistance*
  • Fish Diseases / genetics
  • Fish Diseases / immunology*
  • Intracellular Space / microbiology
  • Intracellular Space / parasitology
  • Piscirickettsia / physiology*
  • Salmo salar / genetics
  • Salmo salar / immunology
  • Salmo salar / microbiology*
  • Salmo salar / parasitology*
  • Stress, Physiological / immunology

Grants and funding

This study was financed by INNOVA-CHILE of CORFO through the projects: 1) Consorcio empresarial de genética y desarrollo biotecnológico para la industria salmonera (N° 206-5047), and 2) Desarrollo de una nueva metodología para la identificación y selección de salmónidos genéticamente resistentes al ectoparásito Caligus rogercresseyi (07CN13PBT-61). This study is a collaborative work of different institutions belonging to “Red de genética e inmunología para el control de patógenos en Acuicultura” (RED CYTED N° 11RT0420). BV received funding from the Ministerio de Economía y Competitividad, Spain (project CGL2012-39861-C02-02). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.