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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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Related in: MedlinePlus

Amoebocyte surface area is higher in sea fans samples during the 2005 bleaching event.Data presented are mean±s.e.m, n = 6, X2 = 24.51, p<0.0001. Asterisk denotes significant differences at p<0.05.
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pone-0001811-g008: Amoebocyte surface area is higher in sea fans samples during the 2005 bleaching event.Data presented are mean±s.e.m, n = 6, X2 = 24.51, p<0.0001. Asterisk denotes significant differences at p<0.05.

Mentions: The average amoebocyte surface area in haphazardly chosen, healthy sea fans was higher during the temperature anomaly than during the year before and after (Figure 8, n = 6, X2 = 24.51, p<0.0001) at the same marked reef site. In 2004 and 2006, the amoebocyte surface area comprised 17% of the coral tissue, approximately the same as in healthy, control sea fans (refer to Figure 5), indicating a stability of the natural unstressed coral amoebocyte populations. In 2005, at the height of the temperature anomaly, the corals had increased amoebocyte surface area to 22% of mesogleal tissue. To confirm temperature as a facilitator of increased amoebocytes, since this was the opposite of our prediction, we experimentally treated sea fan coral clonal replicates to increased water temperatures for 8 days. The increase in amoebocytes was evident in the histological images (Figure 9A and B) and quantified by image analysis (Figure 10, n = 6, X2 = 305.11, p<0.0001.). The coral controls at ambient sea water temperature (27°C–29°C) averaged 16.9% amoebocyte surface area. However, the corals cultured at 31.5°C for 8 days increased their standing amoebocyte concentrations to 29.2%. This increase in amoebocytes was spatially homogenous and systemic within undamaged coral tissue. These data represent the first clear evidence of a systemic reaction to elevated temperature coordinated by the granular amoebocytes.


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)

Amoebocyte surface area is higher in sea fans samples during the 2005 bleaching event.Data presented are mean±s.e.m, n = 6, X2 = 24.51, p<0.0001. 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-g008: Amoebocyte surface area is higher in sea fans samples during the 2005 bleaching event.Data presented are mean±s.e.m, n = 6, X2 = 24.51, p<0.0001. Asterisk denotes significant differences at p<0.05.
Mentions: The average amoebocyte surface area in haphazardly chosen, healthy sea fans was higher during the temperature anomaly than during the year before and after (Figure 8, n = 6, X2 = 24.51, p<0.0001) at the same marked reef site. In 2004 and 2006, the amoebocyte surface area comprised 17% of the coral tissue, approximately the same as in healthy, control sea fans (refer to Figure 5), indicating a stability of the natural unstressed coral amoebocyte populations. In 2005, at the height of the temperature anomaly, the corals had increased amoebocyte surface area to 22% of mesogleal tissue. To confirm temperature as a facilitator of increased amoebocytes, since this was the opposite of our prediction, we experimentally treated sea fan coral clonal replicates to increased water temperatures for 8 days. The increase in amoebocytes was evident in the histological images (Figure 9A and B) and quantified by image analysis (Figure 10, n = 6, X2 = 305.11, p<0.0001.). The coral controls at ambient sea water temperature (27°C–29°C) averaged 16.9% amoebocyte surface area. However, the corals cultured at 31.5°C for 8 days increased their standing amoebocyte concentrations to 29.2%. This increase in amoebocytes was spatially homogenous and systemic within undamaged coral tissue. These data represent the first clear evidence of a systemic reaction to elevated temperature coordinated by the granular amoebocytes.

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