Cellular Responses in Sea Fan Corals: Granular Amoebocytes React to Pathogen and Climate Stressors

Abstract

BackgroundClimate warming is causing environmental change making both marine and terrestrial organisms, and even humans, more susceptible to emerging diseases. Coral reefs are among the most impacted ecosystems by climate stress, and immunity of corals, the most ancient of metazoans, is poorly known. Although coral mortality due to infectious diseases and temperature-related stress is on the rise, the immune effector mechanisms that contribute to the resistance of corals to such events remain elusive. In the Caribbean sea fan corals (Anthozoa, Alcyonacea: Gorgoniidae), the cell-based immune defenses are granular acidophilic amoebocytes, which are known to be involved in wound repair and histocompatibility.Methodology/Principal FindingsWe demonstrate for the first time in corals that these cells are involved in the organismal response to pathogenic and temperature stress. In sea fans with both naturally occurring infections and experimental inoculations with the fungal pathogen Aspergillus sydowii, an inflammatory response, characterized by a massive increase of amoebocytes, was evident near infections. Melanosomes were detected in amoebocytes adjacent to protective melanin bands in infected sea fans; neither was present in uninfected fans. In naturally infected sea fans a concurrent increase in prophenoloxidase activity was detected in infected tissues with dense amoebocytes. Sea fans sampled in the field during the 2005 Caribbean Bleaching Event (a once-in-hundred-year climate event) responded to heat stress with a systemic increase in amoebocytes and amoebocyte densities were also increased by elevated temperature stress in lab experiments.Conclusions/SignificanceThe observed amoebocyte responses indicate that sea fan corals use cellular defenses to combat fungal infection and temperature stress. The ability to mount an inflammatory response may be a contributing factor that allowed the survival of even infected sea fan corals during a stressful climate event.

Nitrogen source preference of Aspergillus sydowii, an infective agent associated with aspergillosis of sea fan corals

“…Despite extensive knowledge of the physical signs (Smith et al 1996), host immune response (Mydlarz et al 2008), and environmental correlates of aspergillosis (Baker et al 2007), the metabolism of sea fan-derived nutrients had not been tested before this study. In this experiment, d 15 N of fungi grown on media containing HSF were on average 1.9% higher than the HSF d 15 N (4.0%; Fig.…”

“…Caused by the terrestrial fungus Aspergillus sydowii (Smith et al 1996;Geiser et al 1998), signs of aspergillosis include galls and lesions that spread throughout the sea fan, killing the tissue and exposing the gorgonin skeleton. Halos of purple tissue surrounding the lesions are the result of an inflammatory immune response by the coral (Ellner et al 2007;Mydlarz et al 2008). On pristine reefs, constitutive levels of sea fan immune defenses are sufficient to prevent infection by A. sydowii (Dube et al 2002), but environmental stressors can weaken coral immune systems (Mydlarz et al 2008), allowing the fungus to invade the sea fan skeleton.…”

“…Halos of purple tissue surrounding the lesions are the result of an inflammatory immune response by the coral (Ellner et al 2007;Mydlarz et al 2008). On pristine reefs, constitutive levels of sea fan immune defenses are sufficient to prevent infection by A. sydowii (Dube et al 2002), but environmental stressors can weaken coral immune systems (Mydlarz et al 2008), allowing the fungus to invade the sea fan skeleton. Histological evidence suggests that the infection spreads through the coral as the fungus grows within the gorgonin skeleton (Ellner et al 2007).…”

Mechanisms of Immune Responses in Cnidarians

“…The mucus contains several protector factors, including serine protease inhibitors with bactericidal activity and antimicrobial peptides (AMPs) . Some cnidarian species, like the octocoral Gorgonia ventalina, have granular amebocytes specialized in phagocytosis, constituting a primary line of defense against the fungus Aspergillus sydowii, a common pathogen in this species (Mydlarz et al, 2008). Additionally, these amebocytes activate the prophenoloxidase enzymatic pathway that promotes the deposition of melanin in the affected zone, forming a barrier against the dispersion of pathogens (Mydlarz et al, 2006).…”

Aspects of the Innate Immune System in the Caribbean Octocoral Swiftia exserta

“…A series of reports by Mydlarz and co-workers has found several phenol oxidase isotypes in extracts of Caribbean corals (Mydlarz, et al, 2008, Mydlarz andPalmer, 2011).…”