Unravelling the different causes of nitrate and ammonium effects on coral bleaching

Abstract

Mass coral bleaching represents one of the greatest threats to coral reefs and has mainly been attributed to seawater warming. However, reduced water quality can also interact with warming to increase coral bleaching, but this interaction depends on nutrient ratios and forms. In particular, nitrate (no 3 −) enrichment reduces thermal tolerance while ammonium (NH 4 +) enrichment tends to benefit coral health. The biochemical mechanisms underpinning the different bleaching responses of corals exposed to DIN enrichment still need to be investigated. Here, we demonstrated that the coral Stylophora pistillata underwent a severe oxidative stress condition and reduced aerobic scope when exposed to NO 3 − enrichment combined with thermal stress. Such condition resulted in increased bleaching intensity compared to a low-nitrogen condition. On the contrary, NH 4 + enrichment was able to amend the deleterious effects of thermal stress by favoring the oxidative status and energy metabolism of the coral holobiont. Overall, our results demonstrate that the opposite effects of nitrate and ammonium enrichment on coral bleaching are related to the effects on corals' energy/ redox status. As nitrate loading in coastal waters is predicted to significantly increase in the future due to agriculture and land-based pollution, there is the need for urgent management actions to prevent increases in nitrate levels in seawater. In addition, the maintenance of important fish stocks, which provide corals with recycled nitrogen such as ammonium, should be favoured. Shallow-water coral reefs owe their ecological success in nutrient-poor tropical waters to the mutualistic symbiosis between corals and photosynthetic dinoflagellates of the family Symbiodiniaceae 1,2. In addition to performing photosynthesis, these dinoflagellates take up dissolved inorganic nutrients such as nitrogen (nitrate, ammonium) and phosphorus from the surrounding water and recycle host metabolic wastes 3-6. In shallow well-illuminated waters, 95% of the photosynthesis products can be translocated to the coral host 7,8. These molecules support the holobiont (symbionts and host) metabolism, and contribute to coral growth, energy storage and reproduction 7,8. The coral-dinoflagellate association is particularly sensitive to thermal stress, with increasing temperatures resulting in the symbiosis breakdown, a phenomenon known as coral bleaching 9. Many coral reefs are expected to be lost due to sea surface temperature rise as a result of global warming and increased frequency in pulse heat stress events, such as El Niño. Indeed, over the period 1871-2017, reefs have experienced unprecedented levels of thermal stress and mass bleaching 10-12. In addition to this global stress, local stressors, such as eutrophication of coastal waters due to human activities, have also been linked to coral reef degradation 13. In particular, elevated concentrations of dissolved inorganic nitrogen (DIN) in seawater have been associated to lower coral thermal tolerance, higher susceptibility to b...

Heat stress destabilizes symbiotic nutrient cycling in corals

“…In this context, previous studies reported that environmental nitrogen availability can affect the bleaching susceptibility of corals ( 31 , 67 ). While moderate increases in seawater NH 4 + concentrations do not impair the symbiosis during heat stress ( 30 , 68 ), increased NO 3 − concentrations reduce translocation of photosynthates by algal symbionts and enhance bleaching susceptibility of corals ( 25 , 69 ). In contrast to NH 4 + , in hospite NO 3 − availability cannot be regulated via symbiotic resource competition as the host lacks the cellular machinery for nitrate reduction ( 70 ).…”

Multi-omic characterization of the thermal stress phenome in the stony coral Montipora capitata

“…That is, in addition to a role in host processes, the coral animal may be dampening algal proliferation by reducing access to nutrients needed for growth such as ammonium, as demonstrated in the cnidarian model Aiptasia under the fully symbiotic stage (27). This hypothesis conflicts with the findings of Fernandes et al (28) who found that ammonium enrichment reduced thermal stress in the coral Stylophora pistillata and supported symbiont stability. This aspect may be less important for Hawaiian M. capitata that meets 100% of its energy needs through heterotrophic feeding during periods of bleaching (7).…”

Increased Ammonium Assimilation Activity in the Scleractinian Coral Pocillopora damicornis but Not Its Symbiont After Acute Heat Stress

“…In the present study, glufosinate could repress the GS activities and corresponding ammonium assimilation ability in the coral host and symbionts, and caused inadequate acquisition of inorganic nitrogen resource for the symbiotic association and earlier collapse of the symbiosis under heat stress, which implied that available ammonium could contribute to the acclimatization of the symbiotic association to heat stress. This was also manifested in some observation that ammonium availability could reduce the negative effect of heat stress on scleractinian corals (Beraud et al, 2013;Zhou et al, 2017;Fernandes de Barros Marangoni et al, 2020). However, the significant decline of symbiont density was only observed at 6 h after the treatment, which could result from the compensation effect of GDH pathway in the coral host.…”