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Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors.

Mydlarz LD, Holthouse SF, Peters EC, Harvell CD - PLoS ONE (2008)

Bottom Line: Melanosomes were detected in amoebocytes adjacent to protective melanin bands in infected sea fans; neither was present in uninfected fans.The 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Texas at Arlington, Arlington, Texas, United States of America. Mydlarz@UTA.edu

ABSTRACT

Background: Climate 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 findings: We 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/significance: The 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.

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Quantitative analysis of amoebocytes in mesoglea of sea fans experimentally exposed to Aspergillus sydowii.A) Increase in amoebocytes in sea fans exposed to fungal hyphae, n = 14, X2 = 41.85, p<0.0001. B) Fine spatial analysis of amoebocyte surface area at point of fungus exposure and 1, 4, and 8 mm away. Dashed line indicated control or basal % amoebocyte surface area. Data presented are mean±s.e.m, n = 8, F = 18.95, p = 0.015. Asterisk denotes significant differences at p<0.05.
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pone-0001811-g006: Quantitative analysis of amoebocytes in mesoglea of sea fans experimentally exposed to Aspergillus sydowii.A) Increase in amoebocytes in sea fans exposed to fungal hyphae, n = 14, X2 = 41.85, p<0.0001. B) Fine spatial analysis of amoebocyte surface area at point of fungus exposure and 1, 4, and 8 mm away. Dashed line indicated control or basal % amoebocyte surface area. Data presented are mean±s.e.m, n = 8, F = 18.95, p = 0.015. Asterisk denotes significant differences at p<0.05.

Mentions: To examine whether the increase in amoebocytes in infected tissue could be experimentally generated, we exposed corals to Aspergillus sydowii grown in culture and measured the amoebocyte response in histological preparations. Application of the fungus in wicks to the surface of the coral caused tissue necrosis and the formation of lesions with exposed coral skeleton that did not occur in sham-inoculated corals. Surrounding the areas of necrosis, amoebocyte surface area increased significantly above sham-inoculated corals. (Figure 6A, n = 14, X2 = 41.85, p<0.0001). Fine spatial scale analysis revealed the increase was localized to the area immediately adjacent to the fungus; just 1 mm away from the lesion amoebocyte concentrations were the same as unaffected tissue (Figure 6B, n = 8, X2 = 18.95, p = 0.0003). While the areas 4 and 8 mm away from the pathogen had fewer amoebocytes than the edge of the lesion, they did not have fewer amoebocytes than the basal levels in control corals, indicating that a simple local migration of amoebocytes to the affected area did not occur. On a larger scale, unaffected tissue (>15 cm away from the lesion) of naturally infected corals did not show an increase in amoebocyte numbers; further evidence against a systemic response (Figure 7, n = 8, X2 = 12.43, p = 0.0004 ). Therefore, in response to A. sydowii invasion both by natural or experimental exposure, the coral amoebocytes are induced to increase locally closest to the areas of infection and pathogen penetration and there is no evidence for a systemic increase.


Cellular responses in sea fan corals: granular amoebocytes react to pathogen and climate stressors.

Mydlarz LD, Holthouse SF, Peters EC, Harvell CD - PLoS ONE (2008)

Quantitative analysis of amoebocytes in mesoglea of sea fans experimentally exposed to Aspergillus sydowii.A) Increase in amoebocytes in sea fans exposed to fungal hyphae, n = 14, X2 = 41.85, p<0.0001. B) Fine spatial analysis of amoebocyte surface area at point of fungus exposure and 1, 4, and 8 mm away. Dashed line indicated control or basal % amoebocyte surface area. Data presented are mean±s.e.m, n = 8, F = 18.95, p = 0.015. Asterisk denotes significant differences at p<0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2267492&req=5

pone-0001811-g006: Quantitative analysis of amoebocytes in mesoglea of sea fans experimentally exposed to Aspergillus sydowii.A) Increase in amoebocytes in sea fans exposed to fungal hyphae, n = 14, X2 = 41.85, p<0.0001. B) Fine spatial analysis of amoebocyte surface area at point of fungus exposure and 1, 4, and 8 mm away. Dashed line indicated control or basal % amoebocyte surface area. Data presented are mean±s.e.m, n = 8, F = 18.95, p = 0.015. Asterisk denotes significant differences at p<0.05.
Mentions: To examine whether the increase in amoebocytes in infected tissue could be experimentally generated, we exposed corals to Aspergillus sydowii grown in culture and measured the amoebocyte response in histological preparations. Application of the fungus in wicks to the surface of the coral caused tissue necrosis and the formation of lesions with exposed coral skeleton that did not occur in sham-inoculated corals. Surrounding the areas of necrosis, amoebocyte surface area increased significantly above sham-inoculated corals. (Figure 6A, n = 14, X2 = 41.85, p<0.0001). Fine spatial scale analysis revealed the increase was localized to the area immediately adjacent to the fungus; just 1 mm away from the lesion amoebocyte concentrations were the same as unaffected tissue (Figure 6B, n = 8, X2 = 18.95, p = 0.0003). While the areas 4 and 8 mm away from the pathogen had fewer amoebocytes than the edge of the lesion, they did not have fewer amoebocytes than the basal levels in control corals, indicating that a simple local migration of amoebocytes to the affected area did not occur. On a larger scale, unaffected tissue (>15 cm away from the lesion) of naturally infected corals did not show an increase in amoebocyte numbers; further evidence against a systemic response (Figure 7, n = 8, X2 = 12.43, p = 0.0004 ). Therefore, in response to A. sydowii invasion both by natural or experimental exposure, the coral amoebocytes are induced to increase locally closest to the areas of infection and pathogen penetration and there is no evidence for a systemic increase.

Bottom Line: Melanosomes were detected in amoebocytes adjacent to protective melanin bands in infected sea fans; neither was present in uninfected fans.The 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Texas at Arlington, Arlington, Texas, United States of America. Mydlarz@UTA.edu

ABSTRACT

Background: Climate 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 findings: We 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/significance: The 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.

Show MeSH
Related in: MedlinePlus