Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata

Reyes-Bermudez, Alejandro; DeSalvo, Michael K.; Voolstra, Christian R.; Sunagawa, Shinichi; Szmant, Alina M.; Iglesias-Prieto, Roberto; Medina, Mónica

doi:10.1016/j.margen.2009.07.002

Cited by 44 publications

(44 citation statements)

References 78 publications

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“…Although previous work has investigated the downstream effectors of apoptosis such as caspases (43) and Bcl-2 family members (42), this is the first examination, to our knowledge, of the upstream ligands and receptors involved with initiating apoptosis in coral. Recently published transcriptomic studies of corals exposed to various environmental stressors have implicated members of the TNFSF/TNFRSF, as well as downstream proteins involved with apoptosis, supporting the ecological relevance of the TNF pathway in coral (45)(46)(47)(48)(49).…”

Section: Discussionmentioning

confidence: 79%

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

Quistad

Stotland

Barott

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The Precambrian explosion led to the rapid appearance of most major animal phyla alive today. It has been argued that the complexity of life has steadily increased since that event. Here we challenge this hypothesis through the characterization of apoptosis in reef-building corals, representatives of some of the earliest animals. Bioinformatic analysis reveals that all of the major components of the death receptor pathway are present in coral with high-predicted structural conservation with Homo sapiens. The TNF receptor-ligand superfamilies (TNFRSF/TNFSF) are central mediators of the death receptor pathway, and the predicted proteome of Acropora digitifera contains more putative coral TNFRSF members than any organism described thus far, including humans. This high abundance of TNFRSF members, as well as the predicted structural conservation of other death receptor signaling proteins, led us to wonder what would happen if corals were exposed to a member of the human TNFSF (HuTNFα). HuTNFα was found to bind directly to coral cells, increase caspase activity, cause apoptotic blebbing and cell death, and finally induce coral bleaching. Next, immortalized human T cells (Jurkats) expressing a functional death receptor pathway (WT) and a corresponding Fas-associated death domain protein (FADD) KO cell line were exposed to a coral TNFSF member (AdTNF1) identified and purified here. AdTNF1 treatment resulted in significantly higher cell death (P < 0.0001) in WT Jurkats compared with the corresponding FADD KO, demonstrating that coral AdTNF1 activates the H. sapiens death receptor pathway. Taken together, these data show remarkable conservation of the TNF-induced apoptotic response representing 550 My of functional conservation. evolution immunity | cytokines | Cnidarians | climate change | invertebrate immunity

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Section: Discussionmentioning

confidence: 79%

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

Quistad

Stotland

Barott

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…DeSalvo et al, 2008;Bay et al, 2009;Császár et al, 2009;Reyes-Bermudez et al, 2009;Voolstra et al, 2009;DeSalvo et al, 2010;Portune et al, 2010;Starcevic et al, 2010;Hoogenboom et al, 2011;Kenkel et al, 2011;Leggat et al, 2011;Levy et al, 2011), generating a wealth of potentially interesting findings with regard to the molecular capacity of corals to acclimate to changes they may face over the Site of origin (SO), temperature treatment (TT) and interaction effects were deemed statistically significant at P<0.05 and, in such cases, are denoted by a tick. Only response variables for which significant differences were detected have been included..…”

Section: Methodological Quality Controlmentioning

confidence: 99%

The effects of a variable temperature regime on the physiology of the reef-building coralSeriatopora hystrix: results from a laboratory-based reciprocal transplant

Mayfield

Chan

Putnam

et al. 2012

Journal of Experimental Biology

104

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SUMMARYTo understand the effects of global climate change on reef-building corals, a thorough investigation of their physiological mechanisms of acclimatization is warranted. However, static temperature manipulations may underestimate the thermal complexity of the reefs in which many corals live. For instance, corals of Houbihu, Taiwan, experience changes in temperature of up to 10°C over the course of a day during spring-tide upwelling events. To better understand the phenotypic plasticity of these corals, a laboratory-based experiment was conducted whereby specimens of Seriatopora hystrix from an upwelling reef (Houbihu) and conspecifics from a non-upwelling reef (Houwan) were exposed to both a stable seawater temperature (26°C) regime and a regime characterized by a 6°C fluctuation (23-29°C) over a 12h period for 7days. A suite of physiological and molecular parameters was measured in samples of both treatments, as well as in experimental controls, to determine site of origin (SO) and temperature treatment (TT) responses. Only chlorophyll a (chl a) concentration and growth demonstrated the hypothesized trend of higher levels when exposed to a TT that mimicked SO conditions. In contrast, chl a, maximum dark-adapted quantum yield of photosystem II (F v /F m ), and Symbiodinium ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL), photosystem I (psI, subunit III) and phosphoglycolate phosphatase (pgpase) mRNA expression demonstrated significant TT effects. Specifically, levels of these response variables were higher in samples exposed to a variable temperature regime, suggesting that S. hystrix may acclimate to fluctuating temperatures by increasing its capacity for photosynthesis.Supplementary material available online at http://jeb.biologists.org/cgi/content/full/215/23/4183/DC1 Key words: acclimation, coral reef, endosymbiosis, gene expression, photosynthesis, Symbiodinium. susceptible to impact by unexpected environmental variability, and results must always be interpreted conservatively.With this in mind, by conducting a laboratory-based reciprocal transplant (LBRT) study, we took advantage of the thermally unique and dynamic environments of southern Taiwan in order to gain insight into how a common reef-building scleractinian, Seriatopora hystrix Dana 1846, acclimates to changes in seawater temperature. Coral colonies were collected from both Houbihu, a reef within Nanwan Bay that experiences episodic summer upwelling (Putnam et al., 2010), and Houwan, a reef on the western side of the Hengchun Peninsula that does not experience this phenomenon, and specimens from each site were incubated at either stable (26°C) or variable (23-29°C over a 12h period) temperature for 7days. This laboratory-based approach was also utilized in place of a reciprocal transplant in situ because of the multitude of other abiotic parameters (e.g. nutrient and dissolved oxygen levels) that are affected by upwelling events in Taiwan (Chen et al., 2004); while the physiological response to upwelling is indeed a worthy avenue ...

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“…Lack of change in relevant symbiont availability within the sediments from the start to the end of the experiment indicates that lack of symbionts available for infection was not the underlying reason, but does suggest that active selection by the host or competition among symbionts was driving temporal changes in community structure. Although developmental changes associated with metamorphosis in other invertebrate systems may be more extreme, skeletogenesis, and developmental changes occurring during the juvenile stage have large impacts on gene expression, differentiating between patterns expressed by larval and adult stages (Reyes-Bermudez et al, 2009). Accordingly, temporal differences and successional patterns in Symbiodinium communities associated with A. tenuis juveniles may be tied to changing requirements associated with the onset of specific physiological processes (e.g., calcification) or changing colony morphology (e.g., the onset of vertical colony growth; Abrego et al, 2009).…”

Section: Predisposition For Up-take Of Specific Symbiodinium Typesmentioning

confidence: 99%

Temperature and Water Quality-Related Patterns in Sediment-Associated Symbiodinium Communities Impact Symbiont Uptake and Fitness of Juveniles in the Genus Acropora

2017

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The majority of corals acquire their photo-endosymbiont Symbiodinium from environmental sources anew each generation. Despite the critical role that environmental availability of Symbiodinium plays in the potential for corals to acclimate and adapt to changing environments, little is known about the diversity of free-living Symbiodinium communities and how variation in these communities influences uptake and in hospite communities in juvenile corals. Here we characterize Symbiodinium community diversity in sediment samples collected from eight reefs representing latitudinal and cross-shelf variation in water quality and temperature regimes. Sediment-associated Symbiodinium communities were then compared to in hospite communities acquired by A. tenuis and A. millepora juveniles following 11-145 days of experimental exposure to sediments from each of the reefs. Communities associated with juveniles and sediments differed substantially, with sediments harboring four times more unique OTUs than juveniles (1,125 OTUs vs. 271). Moreover, only 10.6% of these OTUs were shared between juveniles and sediments, indicating selective uptake by acroporid juveniles. The diversity and abundance of Symbiodinium types differed among sediment samples from different temperature and water quality environments. Symbiodinium communities acquired by juveniles also differed among the sediment treatments, despite juveniles having similar parentage. Moreover, Symbiodinium communities displayed different rates of infection, mortality, and photochemical efficiencies, important traits for coral fitness. This study demonstrates that the biogeography of free-living Symbiodinium types found within sediment reservoirs follows patterns along latitudinal and water quality environmental gradients on the Great Barrier Reef. We also demonstrate a bipartite strategy for Symbiodinium uptake by juvenile corals of two horizontally-transmitting acroporid species, whereby uptake is selective within the constraints of environmental availability.

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Gene expression microarray analysis encompassing metamorphosis and the onset of calcification in the scleractinian coral Montastraea faveolata

Cited by 44 publications

References 78 publications

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

The effects of a variable temperature regime on the physiology of the reef-building coralSeriatopora hystrix: results from a laboratory-based reciprocal transplant

Temperature and Water Quality-Related Patterns in Sediment-Associated Symbiodinium Communities Impact Symbiont Uptake and Fitness of Juveniles in the Genus Acropora

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