Peroxynitrite Generation and Increased Heterotrophic Capacity Are Linked to the Disruption of the Coral–Dinoflagellate Symbiosis in a Scleractinian and Hydrocoral Species

Abstract

Ocean warming is one of the greatest global threats to coral reef ecosystems; it leads to the disruption of the coral–dinoflagellate symbiosis (bleaching) and to nutrient starvation, because corals mostly rely on autotrophy (i.e., the supply of photosynthates from the dinoflagellate symbionts) for their energy requirements. Although coral bleaching has been well studied, the early warning signs of bleaching, as well as the capacity of corals to shift from autotrophy to heterotrophy, are still under investigation. In this study, we evaluated the bleaching occurrence of the scleractinian coral Mussismillia harttii and the hydrocoral Millepora alcicornis during a natural thermal stress event, under the 2015–2016 El Niño influence in three reef sites of the South Atlantic. We focused on the link between peroxynitrite (ONOO−) generation and coral bleaching, as ONOO− has been very poorly investigated in corals and never during a natural bleaching event. We also investigated the natural trophic plasticity of the two corals through the use of new lipid biomarkers. The results obtained first demonstrate that ONOO− is linked to the onset and intensity of bleaching in both scleractinian corals and hydrocorals. Indeed, ONOO− concentrations were correlated with bleaching intensity, with the highest levels preceding the highest bleaching intensity. The time lag between bleaching and ONOO− peak was, however, species-specific. In addition, we observed that elevated temperatures forced heterotrophy in scleractinian corals, as Mu. harttii presented high heterotrophic activity 15 to 30 days prior bleaching occurrence. On the contrary, a lower heterotrophic activity was monitored for the hydrocoral Mi. alicornis, which also experienced higher bleaching levels compared to Mu. hartii. Overall, we showed that the levels of ONOO− in coral tissue, combined to the heterotrophic capacity, are two good proxies explaining the intensity of coral bleaching.

Lipid biomarkers reveal the trophic plasticity of octocorals along a depth gradient

“…For example, R. f. fulvum is a species with unusual biochemical composition and metabolic processes (Trifman et al 2016). In agreement with this observation, our results show that R. f. fulvum presented unusually high SDA concentration and the absence of DPA, which, as of now, is unique for all symbiotic octocorals/scleractinians investigated (Mies et al 2018;Marangoni et al 2019).…”

“…f . fulvum presented unusually high SDA concentration and the absence of DPA, which, as of now, is unique for all symbiotic octocorals/scleractinians investigated (Mies et al 2018; Marangoni et al 2019).…”

“…Since fatty acids composition is often specific to particular groups of organisms (Volkman et al 1989;Imbs et al 2016) and animals are generally unable to produce all necessary fatty acids (Dalsgaard et al 2003;Kabeya et al 2018), their content in coral tissue can give useful information on their autotrophic (symbionts) or heterotrophic (zooplankton) origin. There are several fatty acid markers that can be appropriate to follow autotrophy and heterotrophy in corals (see e.g., Dalsgaard et al 2003;Zhukova and Titlyanov 2003;Treignier et al 2008), but three of them have recently been validated as specific markers of feeding strategies for reef corals (Mies et al 2017(Mies et al , 2018Marangoni et al 2019) and have not been reported to be synthesized de novo (see Kabeya et al 2018;Mies et al 2018). This is the case of stearidonic acid (SDA, 18:4ω3) and docosapentaenoic acid (DPA, 22:5ω3), which are robust tracers of the photosynthetic activity of autotrophs (Papina et al 2003;Treignier et al 2008;Mies et al 2018).…”

Southwestern Atlantic reef-building corals Mussismilia spp. are able to spawn while fully bleached

“…After an intense bleaching event, with low energy supply from autotrophy being available, it would be expected that reproduction would not take place. However, M. hispida and M. harttii are intense heterotrophic feeders that use this feeding mode as a compensation mechanism for the decrease in autotrophy (Mies et al 2018b;Marangoni et al 2019). This trophic plasticity has been demonstrated for other coral species (Anthony and Fabricius 2000;Grottoli et al 2004Grottoli et al , 2006Houlbrèque and Ferrier-Pagès 2009), and may have been crucial in sustaining M. hispida and M. harttii reproduction during this particular bleaching event.…”

South Atlantic Coral Reefs Are Major Global Warming Refugia and Less Susceptible to Bleaching

“…oceanographical environment for the development of coral reefs, thereby selecting resistant species (Leão et al, 2003(Leão et al, , 2008Vasconcelos et al, 2018). This kept acroporids entirely out of the South Atlantic and favored massive species with large corallites, which aid in sediment cleaning and heterotrophic feeding (Logan, 1988;Crabbe and Smith, 2002;Mies et al, 2018;Marangoni et al, 2019). Therefore, South Atlantic corals may represent something of a resistant subset of Caribbean coral diversity.…”