Unravelling the different causes of nitrate and ammonium effects on coral bleaching
1.
Dubinsky, Z. & Jokiel, P. L. Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac. Sci. 48, 313–324 (1994).
Google Scholar
2.
LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580 (2018).
CAS PubMed Google Scholar
3.
Falkowski, P. G., Dubinsky, Z., Muscatine, L. & Porter, J. W. Light and the bioenergetics of a symbiotic coral. Bioscience 34, 705–709 (1984).
CAS Google Scholar
4.
Grover, R., Maguer, J.-F., Reynaud-Vaganay, S. & Ferrier-Pagès, C. Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light, and ammonium concentrations. Limnol. Oceanogr. 47, 782–790 (2002).
ADS Google Scholar
5.
Grover, R., Maguer, J.-F., Allemand, D. & Ferrier-Pagès, C. Nitrate uptake in the scleractinian coral Stylophora pistillata. Limnol. Oceanogr. 48, 2266–2274 (2003).
ADS CAS Google Scholar
6.
Godinot, C., Ferrier-Pagès, C. & Grover, R. Kinetics of phosphate uptake by the scleractinian coral Stylophora pistillata. Limnol. Oceanogr. 54, 1627–1633 (2009).
ADS Google Scholar
7.
Muscatine, L., McCloskey, L. R. & Marian, R. E. Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol. Oceanogr. 26, 601–611 (1981).
ADS CAS Google Scholar
8.
Trembley, P., Grover, R., Maguer, J.-F., Legendre, L. & Ferrier-Pagè, C. Autotrophic carbon budget in coral tissue: a new 13C-based model of photosynthate translocation. J. Exp. Biol. 215, 1384–1393 (2012).
Google Scholar
9.
Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).
ADS CAS PubMed Google Scholar
10.
Claar, D. C., Szostek, L., McDevitt-Irwin, J. M., Schanze, J. J. & Baum, J. K. Global patterns and impacts of El Niño events on coral reefs: A meta-analysis. PLoS ONE 13, e0190957 (2018).
PubMed PubMed Central Google Scholar
11.
Lough, J. M., Anderson, K. D. & Ughes, T. P. Increasing thermal stress for tropical coral reefs: 1871–2017. Sci. Rep. 8, 6079 (2018).
ADS CAS PubMed PubMed Central Google Scholar
12.
Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).
ADS CAS PubMed Google Scholar
13.
Lapointe, B. E., Brewton, R. A., Herren, L. W., Porter, J. W. & Hu, C. Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study. Mar. Biol. 166, 108 (2019).
Google Scholar
14.
Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Chang. 3, 160–164 (2013).
ADS CAS Google Scholar
15.
Burkepile, D. E. et al. Nitrogen identity drives differential impacts of nutrients on coral bleaching and mortality. Ecosystems https://doi.org/10.1007/s10021-019-00433-2 (2019).
Article Google Scholar
16.
Shantz, A. A. & Burkepile, D. E. Context-dependent effects of nutrient loading on the coral-algal mutualism. Ecology 95, 1995–2005 (2014).
PubMed Google Scholar
17.
Nordemar, I., Nyströn, M. & Dizon, R. Effects of elevated seawater temperature and nitrate enrichment on the branching coral Porites cylindrica in the absence of particulate food. Mar. Biol. 142, 669–677 (2003).
CAS Google Scholar
18.
Béraud, E., Gevaert, F., Rottier, C. & Ferrier-Pagès, C. The response of the scleractinian coral Turbinaria reniformis to thermal stress depends on the nitrogen status of the coral holobiont. J. Exp. Biol. 216, 2665–2674 (2013).
PubMed Google Scholar
19.
Ezzat, L., Maguer, J.-F., Grover, R. & Ferrier-Pagès, C. Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean. Sci. Rep. 6, 31768 (2015).
ADS Google Scholar
20.
Lesser, M. P. Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol. Oceanogr. 41, 271–283 (1996).
ADS CAS Google Scholar
21.
Lesser, M. P. Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16, 187–192 (1997).
ADS Google Scholar
22.
Lesser, M. P. Oxidative stress in marine environments: biochemistry and physiological Ecology. Annu. Rev. Physiol. 68, 253–278 (2006).
CAS PubMed Google Scholar
23.
Downs, C. A. et al. Oxidative stress and seasonal coral bleaching. Free Rad. Biol. Med. 33, 533–543 (2002).
CAS PubMed Google Scholar
24.
Perez, S. & Weis, V. Nitric oxide and cnidarians bleaching: an eviction notice mediates breakdown of a symbiosis. J. Exp. Biol. 209, 2804–2810 (2006).
CAS PubMed Google Scholar
25.
Weis, V. M. Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis. J. Exp. Biol. 211, 59–66 (2008).
Google Scholar
26.
Halliwell, B. & Gutteridge, J.M.C. (eds.) Free Radicals in Biology and Medicine. (Oxford, 2007).
27.
Pörtner, H. O. & Farrell, A. P. Physiology and climate change. Science 322, 690–692 (2008).
PubMed Google Scholar
28.
Sokolova, I. M. Energy-Limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integ. Comp. Biol. 53, 597–608 (2013).
Google Scholar
29.
Dominguez-Valdivia, M. D. et al. Nitrogen nutrtion and antioxidant metabolism in ammonium-tolerant and –sensitive plants. Phys. Plant. 132, 359–369 (2008).
CAS Google Scholar
30.
Bouchard, J. N. & Yamasaki, H. Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: a possible linkage between nitric oxide and the coral bleaching phenomenon. Plant. Cell Physiol. 49, 641–652 (2008).
CAS PubMed Google Scholar
31.
Yamasaki, H. & Sakihama, Y. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reducatase: in vitro evidence for the NR*dependent formation of active nitrogen species. FEBS. 468, 89–92 (2000).
CAS Google Scholar
32.
Bethke, P. C., Badger, M. R. & Jones, R. L. Apoplastic synthesis of nitric oxide by plant tissues. Plant. Cell. 16, 332–341 (2004).
CAS PubMed PubMed Central Google Scholar
33.
Tischner, R., Planchet, E. & Kaiser, W. M. Mitochondrial electron transport as a source of nitric oxide in the unicellular green algae Chlorella sorokiniana. FEBS Lett. 576, 151–155 (2004).
CAS PubMed Google Scholar
34.
Planchet, E., Gupta, K. J., Sonoda, M. & Kaiser, W. M. Nitric oxide emission from tabacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant. J. 41, 732–743 (2005).
CAS PubMed Google Scholar
35.
Bartesaghi, S. & Radi, R. Fundamentals on the biochemistry of peroxynitrite and protein tyrosine nitration. Redox. Biol. 14, 618–625 (2018).
CAS PubMed Google Scholar
36.
Brodie, J., Devlin, M., Heynes, D. & Waterhouse, J. Assessment of the eutrophication status of the Great Barrier Reef lagoon (Australia). Biogeochemistry 106, 281–302 (2011).
CAS Google Scholar
37.
Govers, L. L., Lamers, L. P., Bouma, T. J., de Brouwer, J. H. & van Katwijk, M. M. Eutrophication threatens Caribbean seagrass: an example from Curaçao and Bonaire. Mar. Poll. Bull. 89, 481–486 (2014).
CAS Google Scholar
38.
Naumann, M. S., Bednarz, V. N., Ferse, S. C., Niggl, W. & Wild, C. Monitoring of coastal coral reefs near Dahab (Gulf of Aqaba, red sea) indicates local eutrophication as potential cause for change in benthic communities. Environ. Monit. Assess. 187, 1–14 (2015).
CAS Google Scholar
39.
Rouzé, H., Lecellier, G., Langlade, M., Planes, S. & Berteaux-Lecellier, V. Fringing reefs exposed to different levels of eutrophication and sedimentation can support similar benthic communities. Mar. Pollut. Bull. 92, 212–221 (2015).
PubMed Google Scholar
40.
Hoogenboom, M., Beraud, E. & Ferrier-Pagè, C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29, 21–29 (2010).
ADS Google Scholar
41.
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 7, 248–254 (1976).
Google Scholar
42.
Jeffrey, S. & Humphrey, G. New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem. Physiol. Pfl. 167, 191–194 (1975).
CAS Google Scholar
43.
Veal, C. J., Carmi, M., Fine, M. & Hoegh-Guldberg, O. Increasing the accuracy of surface area estimation using single wax dipping of coral fragments. Coral Reefs 29, 893–897 (2010).
ADS Google Scholar
44.
Jones, R. J., Kildea, T. & Hoegh-Guldberg, O. PAM chlorophyll fluorometry: a new in situ technique for stress assessment in scleractinian corals, used to examine the effects of cyanide from cyanide fishing. Mar. Pollut. Bull. 38, 864–874 (1999).
CAS Google Scholar
45.
Jones, R. The ecotoxicological effects of photosystem II herbicides on corals. Mar. Pollut. Bull. 51, 495–506 (2005).
CAS PubMed Google Scholar
46.
Davies, P. S. Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar. Biol. 101, 389–395 (1989).
Google Scholar
47.
Aguiar, R. B. et al. Estradiol valerate and tibolone: effects upon brain oxidative stress and blood biochemistry during aging in female rats. Biogerontology 9, 285–298 (2008).
CAS PubMed Google Scholar
48.
Oakes, K. D. & van der Kraak, G. J. Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat. Toxicol. 63, 447–463 (2003).
CAS PubMed Google Scholar
49.
Huang, D., Ou, B. & Prior, R. L. The chemistry behind antioxidant capacity assays. J. Agric. Food. Chem. 53, 1841–1856 (2005).
CAS PubMed Google Scholar
50.
Sokolova, I. M., Frederich, M., Bagwe, R., Lanning, G. & Sukhotin, A. A. Energy homeostasis as an integrative tool for assessing limits of envirnmental stress tolerance in aquatic organisms. Mar. Environ. Res. 79, 1–15 (2012).
CAS PubMed Google Scholar
51.
Underwood, A. J. Experiments in Ecology: Their Logical Design and Interpretation Using Analysis of Variance (Cambridge University Press, Cambridge, U.K., 1997).
Google Scholar
52.
Halliwell, B. Biochemistry of oxidative stress. Biochem. Soc. Trans. 35, 1147–1150 (2007).
CAS PubMed Google Scholar
53.
Havaux, M. & Niyogi, K. K. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc. Natl. Acad. Sci. USA 96, 8762–8767 (1999).
ADS CAS PubMed Google Scholar
54.
Tardy, F. & Havaux, M. Thylakoid membrane fluidity and thermostability during the operation of the xanthophyll cycle in higher-plant chloroplasts. Biochim. Biophys. Acta. 1330, 179–193 (1997).
CAS PubMed Google Scholar
55.
Downs, C. A., Mueller, E., Phillips, S., Fauth, J. E. & Woodley, C. M. A molecular biomarker system for assessing the health of coral (Montastrea faveolata) during heat stress. Mar. Biotechnol. 2, 533–544 (2000).
CAS PubMed Google Scholar
56.
Krueger, T. et al. Differential coral bleaching—contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress. Comp. Biochem. Physiol. Part A: Mol. Integ. Physiol. 190, 15–25 (2015).
CAS Google Scholar
57.
Marangoni, L. F. B. et al. Oxidative stress biomarkers as potential tools in reef degradation monitoring: a study case in a South Atlantic reef under influence of the 2015–2016 El Niño/Southern Oscillation (ENSO). Ecol. Ind. 106, 105533 (2019).
CAS Google Scholar
58.
Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral-Symbiodiniaceae Symbioses. Trends Microbiol. 8, 678–689 (2019).
Google Scholar
59.
Axenov-Gribanov, D. V. et al. A cellular and metabolic assessment of the thermal stress responses in the endemic gastropod Benedictia limnaeoides ongurensis from Lake Baikal. Comp. Biochem. Physiol. Part B. 167, 16–22 (2013).
Google Scholar
60.
Larade, S. & Storey, K. B. A profile of metabolic responses to anoxia in marine invertebrates. In Sensing, Signaling and Cell Adaptation (eds Storey, K. B. & Storey, J. M.) 27–46 (Elsevier, Amsterdam, 2002).
Google Scholar
61.
Philip, A., Macdonald, A. L. & Watt, P. W. Lactate—a signal coordinating cell and systemic function. J. Exp. Biol. 208, 4561–4575 (2005).
Google Scholar
62.
Riobò, N. A. et al. Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. Biochem. J. 359, 139–145 (2001).
PubMed PubMed Central Google Scholar
63.
Wang, Y. & Ruby, E. G. The roles of NO in microbial symbioses. Cell. Microbiol. 13, 518–526 (2013).
Google Scholar
64.
Higuchi, T., Yuyama, I. & Nakamura, T. The combined effects of nitrate with high temperature and high light intensity on coral bleaching and antioxidant enzyme activities. Reg. S. Mar. Sci. 2, 27–31 (2015).
Google Scholar
65.
Muscatine, L. & Porter, J. W. Reef corals-mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27, 454–460 (1977).
Google Scholar
66.
Ezzat, L., Maguer, J.-F., Grover, R. & Ferrier-Pagès, C. New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4+ and NO3− supply. Proc. R. Soc. B. 282, 20150610 (2015).
PubMed Google Scholar
67.
Cunning, R. & Baker, A. C. Excess algal symbionts increase the susceptibility of reef corals to bleaching. Nat. Clim. Change 3, 259–262 (2013).
ADS Google Scholar
68.
Meyer, J. L. & Schultz, E. T. Migrating haemulid fishes as a source of nutrients and organic matter on coral reefs. Limnol. Oceanogr. 30, 146–156 (1985).
ADS Google Scholar More
