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Exploring the Environmental Physiology of the Indo-Pacific Reef Coral Seriatopora hystrix with Differential Proteomics

DOI: 10.4236/ojms.2018.82012, PP. 223-252

Keywords: Acclimation, Coral Reefs, Dinoflagellate, Environmental Physiology, Marine Biology, Marine Invertebrates, Molecular Biology, Proteomics, Taiwan

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Although reef-building corals are threatened by a number of anthropogenic impacts, certain scleractinian-dinoflagellate (genus Symbiodinium) endosymbioses have proven markedly resilient to environmental change. For instance, corals from upwelling habitats of Southern Taiwan withstand both short- and long-term increases in temperature, potentially due to their routine exposure to highly variable temperature regimes in situ. To gain a greater understanding of the proteomic basis for such acclimatization to unstable environmental conditions, specimens of the Indo-Pacific reef-building coral Seriatopora hystrix Dana 1846 were sampled during a period of stable temperature conditions from 1) a site characterized by frequent upwelling events in Southern Taiwan and 2) a nearby, non-upwelling control site in the Taiwan Strait. Two-dimensional gel electrophoresis followed by sequencing of differentially concentrated proteins with mass spectrometry unveiled significantly more proteins involved in the cellular stress response in coral hosts of the upwelling site. Although such stress protein signatures could be indicative of sub-lethal levels of cellular stress, especially given the relatively higher sediment loads characteristic of the upwelling site, these proteins may, in contrast, have been constitutively maintained at high levels in preparation for large fluctuations in temperature and other abiotic parameters (e.g., nutrient levels) brought upon by upwelling events.


[1]  Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A. and Hatziolos, M.E. (2007) Coral Reefs under Rapid Climate Change and Ocean Acidification. Science, 318, 1737-1742.
[2]  Putnam, H.M., Barott, K., Ainsworth, T.D. and Gates, R.D. (2017) The Vulnerability and Resilience of Reef-Building Corals. Current Biology, 27, R528-R540.
[3]  Brown, B.E. (1997) Coral Bleaching: Causes and Consequences. Coral Reefs, 16, s129-s138.
[4]  Gates, R.D. and Edmunds, P.J. (1999) The Physiological Mechanisms of Acclimatization in Tropical Reef Corals. Integrative and Comparative Biology, 39, 30-43.
[5]  Barshis, D.J., Stillman, J.H., Gates, R.D., Toonen, R.J., Smith, L.W. and Birkeland, C. (2010) Protein Expression and Genetic Structure of the Coral Porites lobata in an Environmentally Extreme Samoan Back Reef: Does Host Genotype Limit Phenotypic Plasticity? Molecular Ecology, 19, 1705-1720.
[6]  Krueger, T., Horwitz, N., Bodin, J., Giovani, M.E., Escrig, S., Meibom, A. and Fine, M. (2017) Common Reef-Building Coral in the Northern Red Sea Resistant to Elevated Temperature and Acidification. Royal Society Open Science, 4, Article ID: 170038.
[7]  Mayfield, A.B., Chen, M., Meng, P.J., Lin, H.J., Chen, C.S. and Liu, P.J. (2013) The Physiological Response of the Reef Coral Pocillopora damicornis to Elevated Temperature: Results from Coral Reef Mesocosm Experiments in Southern Taiwan. Marine and Environmental Research, 86, 1-11.
[8]  Mayfield, A.B., Fan, T.Y. and Chen, C.S. (2013) Physiological Acclimation to Elevated Temperature in a Reef-Building Coral from an Upwelling Environment. Coral Reefs, 32, 909-921.
[9]  Mayfield, A.B., Fan, T.Y. and Chen, C.S. (2013) Real-Time PCR-Based Gene Expression Analysis in the Model Reef-Building Coral Pocillopora damicornis: Insight from a Salinity Stress Study. Platax, 10, 1-29.
[10]  Mayfield, A.B., Chen, C.S. and Liu, P.J. (2014) Decreased Green Fluorescent Protein-Like Chromoprotein Gene Expression in Specimens of the Reef-Building Coral Pocillopora damicornis Undergoing High Temperature-Induced Bleaching. Platax, 11, 1-23.
[11]  Putnam, H.M. and Edmunds, P.J. (2011) The Physiological Response of Reef Corals to Diel Fluctuations in Seawater Temperature. Journal of Experimental Marine Biology and Ecology, 396, 216-223.
[12]  Mayfield, A.B., Chan, P.H., Putnam, H.M., Chen, C.S. and Fan, T.Y. (2012) The Effects of a Variable Temperature Regime on the Physiology of the Reef-Building Coral Seriatopora hystrix: Results from a Laboratory-Based Reciprocal Transplant. Journal of Experimental Biology, 215, 4183-4195.
[13]  Chen, C.T.A., Hsing, L.Y., Liu, C.L. and Wang, S.L. (2004) Degree of Nutrient Consumption of Upwelled Water in the Taiwan Strait Based on Dissolved Organic Phosphorus or Nitrogen. Marine Chemistry, 87, 73-86.
[14]  Mayfield, A.B., Fan, T.Y. and Chen, C.S. (2013) The Physiological Impact of ex Situ Transplantation on the Taiwanese Reef-Building Coral Seriatopora hystrix. Journal of Marine Biology, 2013, Article ID: 569369.
[15]  Mayfield, A.B., Chen, Y.H., Dai, C.F. and Chen, C.S. (2014) The Effects of Temperature on Gene Expression in the Reef-Building Coral Seriatopora hystrix: Insight from Aquarium Studies in Southern Taiwan. International Journal of Marine Science, 4, 1-23.
[16]  Mayfield, A.B., Chen, Y.J., Lu, C.Y. and Chen, C.S. (2016) Proteins Responsive to Variable Temperature Exposure in the Reef-Building Coral Seriatopora hystrix. In: Ortiz, S., Ed., Coral Reefs: Ecosystems, Environmental Impact and Current Threats, NOVA Publishing, New York, 1-60.
[17]  Mayfield, A.B., Wang, Y.B., Chen, C.S., Chen, S.H. and Lin, C.Y. (2016) Dual-Compartmental Transcriptomic + Proteomic Analysis of a Marine Endosymbiosis Exposed to Environmental Change. Molecular Ecology, 25, 5944-5958.
[18]  Peng, S.E., Chen, W.N.U., Chen, H.K., Lu, C.Y., Mayfield, A.B., Fang, L.S. and Chen, C.S. (2011) Lipid Bodies in Coral-Dinoflagellate Endosymbiosis: Ultrastructural and Proteomic Analyses. Proteomics, 17, 3540-3455.
[19]  Weston, A.J., Dunlap, W.C., Shick, J.M., Klueter, A., Iglic, K., Vukelic, A., Starcevic, A., Ward, M., Wells, M.L., Trick, C.G. and Long, P.F. (2012) A Profile of an Endosymbiont-Enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions. Molecular and Cellular Proteomics, 11, M111.015487.
[20]  Oakley, C.A., Ameismeier, M.F., Peng, L., Weis, V.M., Grossman, A.R. and Davy, S.K. (2016) Symbiosis Induces Widespread Changes in the Proteome of the Model Cnidarian Aiptasia. Cellular Microbiology, 18, 1009-1023.
[21]  Weston, A.J., Dunlap, W.C., Beltran, V.H., Starcevic, A., Hranueli, D., Ward, M. and Long, P.F. (2015) Proteomics Links the Redox State to Calcium Signaling during Bleaching of the Scleractinian Coral Acropora microphthalma on Exposure to High Solar Irradiance and Thermal Stress. Molecular and Cellular Proteomics, 14, 585-595.
[22]  Liu, P.J., Meng, P.J., Liu, L.L., Wang, J.T. and Leu, M.Y. (2012) Impacts of Human Activities on Coral Reef Ecosystems of Southern Taiwan: A Long-Term Study. Marine Pollution Bulletin, 64, 1129-1135.
[23]  Ribas-Deulofeu, L., Denis, V., De Palmas, S., Kuo, C.Y., Hsieh, H.J. and Chen, C.A. (2016) Structure of Benthic Communities along the Taiwan Latitudinal Gradient. PLoS ONE, 11, e0160601.
[24]  Tkachenko, K.S., Wu, B.J., Fang, L.S. and Fan, T.Y. (2007) Dynamics of a Coral Reef Community after Mass Mortality of Branching Acropora Corals and an Outbreak of Anemones. Marine Biology, 151, 185-194.
[25]  Mayfield, A.B., Wang, L.H., Tang, P.C., Hsiao, Y.Y., Fan, T.Y., Tsai, C.L. and Chen, C.S. (2011) Assessing the Impacts of Experimentally Elevated Temperature on the Biological Composition and Molecular Chaperone Gene Expression of a Reef Coral. PLoS ONE, 6, e26529.
[26]  Mayfield, A.B., Chen, Y.J., Lu, C.Y. and Chen, C.S. (2018) The Proteomic Response of the Reef Coral Pocillopora acuta to Experimentally Elevated Temperature. PLoS ONE, 13, e0192001.
[27]  Mayfield, A.B. (2016) Uncovering Spatio-Temporal and Treatment-Derived Differences in the Molecular Physiology of a Model Coral-Dinoflagellate Mutualism with Multivariate Statistical Approaches. Journal of Marine Science and Engineering, 4, 63.
[28]  Kim, S. and Pevzner, P.A. (2014) MS-GF+ Makes Progress towards a Universal Database Search Tool for Proteomics. Nature Communication, 5, 5277.
[29]  Chiva, C., Ortega, M. and Sabido, E. (2014) Influence of the Digestion Technique, Protease, and Missed Cleavage Peptides in Protein Quantitation. Journal of Proteome Research, 13, 3979-3986.
[30]  Rudnick, P.A., Markey, S.P., Roth, J., Mirokhin, Y., Yan, X., Tchekhovskoi, D.V., Edwards, N.J., Thangudu, R.R., Ketchum, K.A., Kinsinger, C.R., Mesri, M., Rodriguez, H. and Stein, S. (2016) A Description of the Clinical Proteomic Tumor Analysis Consortium (CPTAC) Common Data Analysis Pipeline. Journal of Proteome Research, 15, 1023-1032.
[31]  Mayfield, A.B., Hsiao, Y.Y., Fan, T.Y. and Chen, C.S. (2012) Temporal Variation in RNA/DNA and Protein/DNA Ratios in Four Anthozoan-Dinoflagellate Endosymbioses of the Indo-Pacific: Implications for Molecular Diagnostics. Platax, 9, 1-24.
[32]  Chen, H.K., Song, S.N., Wang, L.H., Mayfield, A.B., Chen, Y.J., Chen, W.N.U. and Chen, C.S. (2015) A Compartmental Comparison of Major Lipid Species in a Coral-Symbiodinium Endosymbiosis: Evidence That the Coral Host Regulates Lipogenesis of Its Cytosolic Lipid Bodies. PLoS ONE, 10, e0132519.
[33]  Chen, W.N.U., Hsiao, Y.J., Mayfield, A.B., Young, R., Hsu, L., Chen, C.S. and Peng, S.E. (2016) Vertical Transmission of Heterologous Clade C Symbiodinium in a Model Anemone Infection System. Peer J, 4, e2358.
[34]  Chen, H.K., Mayfield, A.B., Wang, L.H. and Chen, C.S. (2017) Coral Lipid Bodies as the Relay Center Interconnecting Diel-Dependent Lipidomic Changes in Different Cellular Compartments. Scientific Reports, 7, 3244.
[35]  Mayfield, A.B., Chen, C.S., Dempsey, A.C. and Bruckner, A.W. (2016) The Molecular Ecophysiology of Closely Related Pocilloporids from the South Pacific: A Case Study from the Austral and Cook Islands. Platax, 13, 1-25.
[36]  Mayfield, A.B., Chen, C.S. and Dempsey, A.C. (2017) Biomarker Profiling in Reef Corals of Tonga’s Ha’apai and Vava’u Archipelagos. PLoS ONE, 12, e0185857.
[37]  Mayfield, A.B., Chen, C.S. and Dempsey, A.C. (2017) Identifying Corals Displaying Aberrant Behavior in Fiji’s Lau Archipelago. PLoS ONE, 12, e0177267.
[38]  Cantwell, R.E. and Hofmann, R. (2011) Ultraviolet Absorption Properties of Suspended Particulate Matter in Untreated Surface Waters. Water Research, 45, 1322-1328.
[39]  Lesser, M.P. (1996) Elevated Temperatures and Ultraviolet Radiation Cause Oxidative Stress and Inhibit Photosynthesis in Symbiotic Dinoflagellates. Limnology and Oceanography, 41, 271-283.
[40]  Lundgren, P., Vera, J.C., Peplow, L., Manel, S. and van Oppen, M.J.H. (2013) Genotype-Environment Correlations in Corals from the Great Barrier Reef. BMC Genetics, 14, 9.
[41]  Meyer, E., Davies, S., Wang, S., Willis, B.L., Abrego, D., Juenger, T.E. and Matz, M.V. (2009) Genetic Variation in Responses to a Settlement Cue and Elevated Temperature in the Reef-Building Coral Acropora millepora. Marine Ecology Progress Series, 392, 81-92.
[42]  Barshis, D.J., Ladner, J.T., Oliver, T.A., Seneca, F.O., Traylor-Knowles, N. and Palumbi, S.R. (2013) Genomic Basis for Coral Resilience to Climate Change. Proceedings of the National Academy of Sciences of the United States of America, 110, 1387-1392.
[43]  Hochachka, P.W. and Somero, G.N. (2002) Biochemical Adaptation. Oxford University Press, Oxford.
[44]  Dong, Y., Miller, L.P., Sanders, J.G. and Somero, G.N. (2008) Heat-Shock Protein 70 (Hsp70) Expression in Four Limpets of the Genus Lottia: Interspecific Variation in Constitutive and Inducible Synthesis Correlates with in Situ Exposure to Heat Stress. The Biological Bulletin, 215, 173-181.
[45]  Fabricius, K.E. (2005) Effects of Terrestrial Run of on the Ecology of Corals and Coral Reefs: Review and Synthesis. Marine Pollution Bulletin, 50, 125-146.
[46]  Liu, P.J., Hsin, M.C., Huang, Y.H., Fan, T.Y., Meng, P.J., Lu, C.C. and Lin, H.J. (2015) Nutrient Enrichment Coupled with Sedimentation Favors Sea Anemones over Corals. PLoS ONE, 10, e0125175.
[47]  Mayfield, A.B. and Gates, R.D. (2007) Osmoregulation in Anthozoan-Dinoflagellate Symbiosis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 147, 1-10.
[48]  Jones, R.J., Hoegh-Guldberg, O., Larkum, A.W.D. and Schreiber, U. (1998) Temperature-Induced Bleaching of Corals Begins with Impairment of the CO2 Fixation Metabolism in Zooxanthellae. Plant, Cell and Environment, 21, 1219-1230.
[49]  Mayfield, A.B., Hsiao, Y.Y., Fan, T.Y., Chen, C.S. and Gates, R.D. (2010) Evaluating the Temporal Stability of Stress-Activated Protein Kinase and Cytoskeleton Gene Expression in the Pacific Corals Pocillopora damicornis and Seriatopora hystrix. Journal of Experimental Marine Biology and Ecology, 395, 215-222.
[50]  Thirone, A.C.P., Speight, P., Zulys, M., Rotstein, O.D., Szaszi, K., Pedersen, S.F. and Kapus, A. (2009) Hyperosmotic Stress Induces Rho/Rho Kinase/LIM Kinase-Mediated Cofilin Phosphorylation in Tubular Cells: Key Role in the Osmotically Triggered F-Actin Response. American Journal of Physiology-Cell Physiology, 296, C463-C475.
[51]  Desalvo, M.K., Voolstra, C.R., Sunagawa, S., Schwarz, J., Stillman, J.H., Coffroth, M.A., Szmant-Froelich, A.M. and Medina, M. (2008) Differential Gene Expression during Thermal Stress and Bleaching in the Caribbean Coral Montastraea faveolata. Molecular Ecology, 17, 3952-3971.
[52]  Palumbi, S.R., Barshis, D.J., Traylor-Knowles, N. and Bay, R.A. (2014) Mechanisms of Reef Coral Resistance to Future Climate Change. Science, 344, 895-898.
[53]  Mayfield, A.B., Wang, Y.B., Chen, C.S., Chen, S.H. and Lin, C.Y. (2014) Compartment-Specific Transcriptomics in a Reef-Building Coral Exposed to Elevated Temperatures. Molecular Ecology, 23, 5816-5830.
[54]  Downs, C.A., Mueller, E., Phillips, S., Fauth, J.E. and Woodley, C.M. (2000) A Molecular Biomarker System for Assessing the Health of Coral (Montastrea faveolata) during Heat Stress. Marine Biotechnology, 2, 533-544.
[55]  Mayfield, A.B., Hirst, M.B. and Gates, R.D. (2009) Gene Expression Normalization in a Dual-Compartment System: A Real-Time PCR Protocol for Symbiotic Anthozoans. Molecular Ecology Resources, 9, 462-470.
[56]  Putnam, H.M., Mayfield, A.B., Fan, T.Y., Chen, C.S. and Gates, R.D. (2013) The Physiological and Molecular Responses of Larvae from the Reef-Building Coral Pocillopora damicornis Exposed to Near-Future Increases in Temperature & pCO2. Marine Biology, 160, 2157-2173.


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