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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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Histological images of sea fans infected with Aspergillus sydowii and presence of melanin both as a band and in amoebocytes as melanosomes.A) Histological preparation of an infected coral stained with H&E showing individual fungal hyphae (F) in skeleton and surrounded by melanin (M). Note granular amoebocytes (ga) aggregated near melanin and fungal hyphae. Scale bar = 25 µm. B) Histological preparation of an infected coral showing multiple amoebocytes containing melanin granules in contact with the thick layer of melanin preventing A. sydowii hyphae within the axial skeleton (at left) from contacting the sea fan tissue (on right). Fontana-Masson staining procedure, scale bar = 25 µm. C) Close up of an amoebocyte containing melanin granules (Mg) and black stained melanin (M) layer surrounding fungus (F). Fontana-Masson staining procedure, scale bar = 10 µm D) Uninfected coral stained with Fontana-Masson's procedure showing lack of melanin and melanin granules. Scale bar = 10 µm.
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pone-0001811-g004: Histological images of sea fans infected with Aspergillus sydowii and presence of melanin both as a band and in amoebocytes as melanosomes.A) Histological preparation of an infected coral stained with H&E showing individual fungal hyphae (F) in skeleton and surrounded by melanin (M). Note granular amoebocytes (ga) aggregated near melanin and fungal hyphae. Scale bar = 25 µm. B) Histological preparation of an infected coral showing multiple amoebocytes containing melanin granules in contact with the thick layer of melanin preventing A. sydowii hyphae within the axial skeleton (at left) from contacting the sea fan tissue (on right). Fontana-Masson staining procedure, scale bar = 25 µm. C) Close up of an amoebocyte containing melanin granules (Mg) and black stained melanin (M) layer surrounding fungus (F). Fontana-Masson staining procedure, scale bar = 10 µm D) Uninfected coral stained with Fontana-Masson's procedure showing lack of melanin and melanin granules. Scale bar = 10 µm.

Mentions: To determine the potential role of the amoebocytes in arresting infections and in melanin biosynthesis, we examined histological preparations of infected sea fans as well as activity of prophenoloxidase. In cross sections stained with hematoxylin and eosin (H&E) fungal hyphae can be seen infiltrating the proteinaceous gorgonin axis, and infected areas of axis are surrounded by layers of host-produced melanin as well as granular amoebocytes (Figure 4A). In addition, we used the Fontana-Masson staining procedure which causes melanin to appear black as a result of the reduction of silver nitrate to metallic silver [29], [30]. In Fontana–Masson stained sections, the layers of melanin surrounding the fungus in the skeleton appear black, furthermore, black granules (melanosome-like) can be seen in the granular amoebocytes (Figures 4B, 4C). No black precipitate is seen in non-infected controls (Figure 4D). Concomitant with melanin deposits and granular amoebocytes is a two-fold increase in prophenoloxidase activity as measured by oxidation of L-dopa to the colored dopachrome in infected tissue (Figure 5, n = 12, F = 4.7, p = 0.04).


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)

Histological images of sea fans infected with Aspergillus sydowii and presence of melanin both as a band and in amoebocytes as melanosomes.A) Histological preparation of an infected coral stained with H&E showing individual fungal hyphae (F) in skeleton and surrounded by melanin (M). Note granular amoebocytes (ga) aggregated near melanin and fungal hyphae. Scale bar = 25 µm. B) Histological preparation of an infected coral showing multiple amoebocytes containing melanin granules in contact with the thick layer of melanin preventing A. sydowii hyphae within the axial skeleton (at left) from contacting the sea fan tissue (on right). Fontana-Masson staining procedure, scale bar = 25 µm. C) Close up of an amoebocyte containing melanin granules (Mg) and black stained melanin (M) layer surrounding fungus (F). Fontana-Masson staining procedure, scale bar = 10 µm D) Uninfected coral stained with Fontana-Masson's procedure showing lack of melanin and melanin granules. Scale bar = 10 µm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0001811-g004: Histological images of sea fans infected with Aspergillus sydowii and presence of melanin both as a band and in amoebocytes as melanosomes.A) Histological preparation of an infected coral stained with H&E showing individual fungal hyphae (F) in skeleton and surrounded by melanin (M). Note granular amoebocytes (ga) aggregated near melanin and fungal hyphae. Scale bar = 25 µm. B) Histological preparation of an infected coral showing multiple amoebocytes containing melanin granules in contact with the thick layer of melanin preventing A. sydowii hyphae within the axial skeleton (at left) from contacting the sea fan tissue (on right). Fontana-Masson staining procedure, scale bar = 25 µm. C) Close up of an amoebocyte containing melanin granules (Mg) and black stained melanin (M) layer surrounding fungus (F). Fontana-Masson staining procedure, scale bar = 10 µm D) Uninfected coral stained with Fontana-Masson's procedure showing lack of melanin and melanin granules. Scale bar = 10 µm.
Mentions: To determine the potential role of the amoebocytes in arresting infections and in melanin biosynthesis, we examined histological preparations of infected sea fans as well as activity of prophenoloxidase. In cross sections stained with hematoxylin and eosin (H&E) fungal hyphae can be seen infiltrating the proteinaceous gorgonin axis, and infected areas of axis are surrounded by layers of host-produced melanin as well as granular amoebocytes (Figure 4A). In addition, we used the Fontana-Masson staining procedure which causes melanin to appear black as a result of the reduction of silver nitrate to metallic silver [29], [30]. In Fontana–Masson stained sections, the layers of melanin surrounding the fungus in the skeleton appear black, furthermore, black granules (melanosome-like) can be seen in the granular amoebocytes (Figures 4B, 4C). No black precipitate is seen in non-infected controls (Figure 4D). Concomitant with melanin deposits and granular amoebocytes is a two-fold increase in prophenoloxidase activity as measured by oxidation of L-dopa to the colored dopachrome in infected tissue (Figure 5, n = 12, F = 4.7, p = 0.04).

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