Despite progress in the past decade, researchers struggle to evaluate the hypothesis that environmental conditions compromise immunity and facilitate new disease outbreaks. In this chapter, we review known immunological mechanisms for selected phyla and find that there are critical response pathways common to all invertebrates. These include the prophenoloxidase pathway, wandering phagocytic cells, cytotoxic effector responses, and antimicrobial compounds. To demonstrate the links between immunity and the environment, we summarize mechanisms by which immunity is compromised by environmental conditions. New environmental challenges may promote emergent disease both through compromised host immunity and introduction of new pathogens. Such challenges include changing climate, polluted environment, anthropogenically facilitated pathogen invasion, and an increase in aquaculture. The consequences of these environmental issues already manifest themselves as increased mortality on coral reefs, pathogen range expansion, and transmission of disease from aquaculture to natural populations, as we summarize in a final section on recent marine epizootics.
Humans are changing the environmental conditions of our planet, and animal immune functions are being affected by these modifications. For instance, a diversity of chemical contaminants is entering ecosystems and modifying immune functions directly or indirectly through altered host-parasite interactions. Also, global temperature changes have caused outbreaks of disease that have decimated and even extirpated some host species, outcomes partially driven via immune alterations. Finally, some invasive species are immunologically distinct or impose stress on native species, factors that may facilitate the establishment of nonnative hosts as well as parasite transmission to native species. Here, we summarize the known and likely effects of pollutants, nonnative species introductions, and increases in ambient temperature on host immune functions and infections. We then identify future directions for research given our sparse knowledge of immune variation in natural populations. In sum, we advocate integrative, multidisciplinary work at diverse spatial and temporal scales to assess and prevent anthropogenic global changes from further compromising animal immune functions.
Climate change is negatively affecting the stability of natural ecosystems, especially coral reefs. The dissociation of the symbiosis between reef-building corals and their algal symbiont, or coral bleaching, has been linked to increased sea surface temperatures. Coral bleaching has significant impacts on corals, including an increase in disease outbreaks that can permanently change the entire reef ecosystem. Yet, little is known about the impacts of coral bleaching on the coral immune system. In this study, whole transcriptome analysis of the coral holobiont and each of the associate components (i.e. coral host, algal symbiont and other associated microorganisms) was used to determine changes in gene expression in corals affected by a natural bleaching event as well as during the recovery phase. The main findings include evidence that the coral holobiont and the coral host have different responses to bleaching, and the host immune system appears suppressed even a year after a bleaching event. These results support the hypothesis that coral bleaching changes the expression of innate immune genes of corals, and these effects can last even after recovery of symbiont populations. Research on the role of immunity on coral's resistance to stressors can help make informed predictions on the future of corals and coral reefs.
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.
Increasing evidence of links between climate change, anthropogenic stress and coral disease underscores the importance of understanding the mechanisms by which reef-building corals resist infection and recover from injury. Cellular inflammation and melanin-producing signalling pathway are two mechanisms employed by invertebrates to remove foreign organisms such as pathogens, but they have not been recorded previously in scleractinian corals. This study demonstrates the presence of the phenoloxidase (PO) activating melanin pathway in two species of coral, Acropora millepora and a massive species of Porites, which both develop local pigmentation in response to interactions with a variety of organisms. L-DOPA (3-(3,4-dihydroxyphenyl)-Lalanine) substrate-based enzyme activation assays demonstrated PO activity in healthy tissues of both species and upregulation in pigmented tissues of A. millepora. Histological staining conclusively identified the presence of melanin in Porites tissues. These results demonstrate that the PO pathway is active in both coral species. Moreover, the upregulation of PO activity in areas of non-normal pigmentation in A. millepora and increased melanin production in pigmented Porites tissues suggest the presence of a generalized defence response to localized stress. Interspecific differences in the usage of pathways involved in innate immunity may underlie the comparative success of massive Porites sp. as long-lived stress tolerators.
BackgroundA wide array of fluorescent proteins (FP) is present in anthozoans, although their biochemical characteristics and function in host tissue remain to be determined. Upregulation of FP's frequently occurs in injured or compromised coral tissue, suggesting a potential role of coral FPs in host stress responses.Methodology/Principal FindingsThe presence of FPs was determined and quantified for a subsample of seven healthy Caribbean coral species using spectral emission analysis of tissue extracts. FP concentration was correlated with the in vivo antioxidant potential of the tissue extracts by quantifying the hydrogen peroxide (H2O2) scavenging rates. FPs of the seven species varied in both type and abundance and demonstrated a positive correlation between H2O2 scavenging rate and FP concentration. To validate this data, the H2O2 scavenging rates of four pure scleractinian FPs, cyan (CFP), green (GFP), red (RFP) and chromoprotein (CP), and their mutant counterparts (without chromophores), were investigated. In vitro, each FP scavenged H2O2 with the most efficient being CP followed by equivalent activity of CFP and RFP. Scavenging was significantly higher in all mutant counterparts.Conclusions/SignificanceBoth naturally occurring and pure coral FPs have significant H2O2 scavenging activity. The higher scavenging rate of RFP and the CP in vitro is consistent with observed increases of these specific FPs in areas of compromised coral tissue. However, the greater scavenging ability of the mutant counterparts suggests additional roles of scleractinian FPs, potentially pertaining to their color. This study documents H2O2 scavenging of scleractinian FPs, a novel biochemical characteristic, both in vivo across multiple species and in vitro with purified proteins. These data support a role for FPs in coral stress and immune responses and highlights the multi-functionality of these conspicuous proteins.
One prominent hypothesis regarding climate change and scleractinian corals is that thermal stress compromises immune competence. To test this hypothesis we tracked how the immune defenses of bleached, apparently healthy and yellow band disease (YBD) diseased Montastraea faveolata colonies varied with natural thermal stress in southwestern Puerto Rico. Colonies were monitored for 21 mo from the peak of the bleaching event in October 2005 to August 2007. Since sea surface temperature was significantly higher in summer and fall 2005 than 2006, year of collection was used as a proxy for temperature stress, and colony fragments collected in 2005 were compared with those collected in 2006. Mortality rate was high (43% overall) and all colonies (except one) either died or became infected with YBD by August 2007. YBD-infected tissue did not bleach (i.e. expel zooxanthellae) during the 2005 bleaching event, even when healthy tissue of these colonies bleached. Immune activity was assayed by measuring prophenoloxidase (PPO), peroxidase (POX), lysozyme-like (LYS) and antibacterial (AB) activity. Immune activity was variable between all coral samples, but there was a significant elevation of PPO activity in bleached colonies collected in 2005 relative to apparently healthy and YBD-diseased corals in 2006. In YBD-diseased colonies, LYS and AB activity were elevated in both healthy and infected tissue, indicating a systemic response; activity levels in these colonies were higher compared to those that appeared healthy. In both these immune parameters, there was a trend for suppression of activity in corals that were bleached in 2005. These data, while complicated by between-genet variability, illustrate the complex interaction between disease and temperature stress on immune function.
As ocean temperatures rise, investigations into what the physiological effects will be on the symbiotic microalga Symbiodinium, and how these may play into the cnidarian bleaching response, have highlighted the contribution of reactive oxygen species (ROS). Previous studies have laid this groundwork using a limited number of Symbiodinium phylotypes, and so this study aims to expand this understanding by exploring the effects of sub-lethal elevated temperatures on the physiological response of seven genetically distinct types of Symbiodinium, including A1, B1, B2, C1, D, E1, and F2. The production of ROS (at 26 °C, 29 °C, 30 °C, and 31 °C) and activity of the antioxidants catalase (CAT) and superoxide dismutase (SOD) (at 26 °C and 31 °C) were measured as indicators of sensitivity or tolerance to heat stress. Symbiodinium types B1 and C1 were the most thermally sensitive, with C1 producing the highest amount of ROS at elevated temperatures. Types A1 and F2 were tolerant, having no increase in ROS production, and were the only types to increase both CAT and SOD activity with temperature stress. Type B2 had decreased ROS production and elevation of CAT activity, while type E1 had decreased levels of ROS production at elevated temperatures. Type D was the only Symbiodinium type to remain unaffected by elevated temperatures. These results are consistent with previous findings of relative sensitivity or tolerance to elevated temperatures, specifically with regards to types A1, B1, and F2. The inclusion of types B2, C1, D, and E1 provides further new evidence of how types differ in their thermal responses, suggesting differing mechanisms exist in the Symbiodnium response to higher temperature and highlighting the importance of establishing symbiont identity when exploring the response of intact associations to this type of stress.
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