Defending against pathogens – immunological priming and its molecular basis in a sea anemone, cnidarian

Abstract

Cnidarians, in general, are long-lived organisms and hence may repeatedly encounter common pathogens during their lifespans. It remains unknown whether these early diverging animals possess some type of immunological reaction that strengthens the defense response upon repeated infections, such as that described in more evolutionary derived organisms. Here we show results that sea anemones that had previously encountered a pathogen under sub-lethal conditions had a higher survivorship during a subsequently lethal challenge than naïve anemones that encountered the pathogen for the first time. Anemones subjected to the lethal challenge two and four weeks after the sub-lethal exposure presented seven- and five-fold increases in survival, respectively, compared to the naïve anemones. However, anemones challenged six weeks after the sub-lethal exposure showed no increase in survivorship. We argue that this short-lasting priming of the defense response could be ecologically relevant if pathogen encounters are restricted to short seasons characterized by high stress. Furthermore, we discovered significant changes in proteomic profiles between naïve sea anemones and those primed after pathogen exposure suggesting a clear molecular signature associated with immunological priming in cnidarians. Our findings reveal that immunological priming may have evolved much earlier in the tree of life than previously thought.

Sea anemone model has a single Toll-like receptor that can function in pathogen detection, NF-κB signal transduction, and development

“…3B and Fig. S1) (28,49). The corals and the anemone A. pallida in which V. coralliilyticus has previously been shown to cause lethal disease are all tropical cnidarians with obligate algal symbionts (26,28,49).…”

“…S1) (28,49). The corals and the anemone A. pallida in which V. coralliilyticus has previously been shown to cause lethal disease are all tropical cnidarians with obligate algal symbionts (26,28,49). In contrast, N. vectensis does not have any known essential symbiont and can live in a variety of habitats over a wide range of environmental conditions (e.g., salinity, pH, temperature) (31).…”

“…V. coralliilyticus is a coral pathogen that is of interest because of its broad host range among corals and its temperature-dependent pathogenicity (27). Recently, V. coralliilyticus was also shown to induce a lethal disease in the symbiotic sea anemone A. pallida (28). To determine whether V. coralliilyticus can induce disease in N. vectensis, anemones were exposed to increasing concentrations of V. coralliilyticus at 30°C.…”

“…One bacterial pathogen that impacts several cnidarian species is the Gram-negative bacterium Vibrio coralliilyticus. Initially described as the causative agent of white syndrome disease in corals, V. coralliilyticus has recently been shown also to cause disease in the tropical sea anemone Aiptasia pallida (26)(27)(28). Although not pathogenic at water temperatures below 24°C, V. coralliilyticus photoinactivates coral symbionts between temperatures 24°C and 26.5°C (27,29).…”

“…Although not pathogenic at water temperatures below 24°C, V. coralliilyticus photoinactivates coral symbionts between temperatures 24°C and 26.5°C (27,29). Above 27°C, V. coralliilyticus is highly pathogenic due to its ability to lyse coral and anemone tissues (27,28,30). As global ocean temperatures rise, the temperature-dependent pathogenicity of V. coralliilyticus threatens many coral species.…”