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)

Marangoni, Laura Fernandes de Barros; Dalmolin, Camila; Marques, Joseane Aparecida; Klein, Roberta Daniele; Abrantes, Douglas P.; Pereira, Cristiano Macedo; Calderón, Emiliano Nicolas; Castro, Clovis B.; Bianchini, Adalto

doi:10.1016/j.ecolind.2019.105533

Cited by 23 publications

(10 citation statements)

References 44 publications

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“…Our results are in agreement with previous evidence showing that NH 4 + enrichment can enlarge symbiont populations whilst also increasing thermal tolerance in corals, and that NO 3 − enrichment can increase bleaching susceptibility without prior symbiont density enlargement 16 . Our findings also agree with the assertion of Morris et al 57 who suggested that the different impacts of ammonium and nitrate on coral thermal tolerance can be explained by their relative effects on the carbon metabolism and oxidative stress of the coral holobiont. We indeed showed that while nitrate enrichment increases oxidative stress in corals, ammonium enrichment tends to decrease it.…”

Section: Discussionsupporting

confidence: 93%

“…As shown in previous work 55 – 57 , thermal stress alone induced oxidative stress in corals, which was evidenced by increasing ROS, TAC and PTN. In accordance, physiological measurements in our study indicated the onset of coral bleaching (decreased symbiont density, chlorophyll a content and photosynthetic efficiency) followed by decreased calcification rates.…”

Section: Discussionsupporting

confidence: 77%

“…Our findings also agree with the assertion of Morris et al . 57 who suggested that the different impacts of ammonium and nitrate on coral thermal tolerance can be explained by their relative effects on the carbon metabolism and oxidative stress of the coral holobiont. We indeed showed that while nitrate enrichment increases oxidative stress in corals, ammonium enrichment tends to decrease it.…”

Section: Discussionmentioning

confidence: 99%

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

Marangoni

Ferrier‐Pagés

Rottier

et al. 2020

Sci Rep

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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...

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

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

Marangoni

Ferrier‐Pagés

Rottier

et al. 2020

Sci Rep

Self Cite

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“…LPO reflects the structural integrity of the cell membranes and production of LPOs indicates that levels of ROS are overwhelming the antioxidant pathways, accumulating and damaging cellular membrane lipids, thus signaling an ongoing oxidative stress (Lesser, 2006;Weis, 2008). An increase of LPO in response to heat stress-inducing bleaching has been widely observed in corals (Downs et al, 2000;Flores-Ramírez and Liñán-Cabello, 2006;Dias et al, 2019a,b;Marangoni et al, 2019a). The increase of both Hsps and LPO in control samples following heat stress coincided with a significant decrease of symbiont density, chlorophyll concentration, and photosynthetic rate, measured previously on the same coral samples (Biscéré et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Manganese Benefits Heat-Stressed Corals at the Cellular Level

et al. 2021

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The intensity and frequency of coral bleaching events have increased worldwide especially due to thermal stress and seawater pollution. Although it has been observed that metal concentration in seawater can affect the coral’s ability to adopt cellular defensive mechanisms to counteract bleaching, more investigations are needed to better understand the role of metals in coral physiology. In this study, we analyzed the individual and combined effects of prolonged heat stress and manganese (Mn) and iron (Fe) enrichments at the cellular level on the coral Stylophora pistillata. Thermal stress caused an up-regulation in the expression of the host Heat shock proteins (Hsps) 60 and 70, which showed a parallel pattern of modulation in all treatments, as well as an increase of lipid peroxidation (LPO) in the holobiont. Fe enrichment did not induce any change in Hsp expression or in the oxidative status of the corals both at the ambient temperature of 26°C or at increased temperature, suggesting that Fe didn’t seem to play a role in mitigating the cellular damages and the coral bleaching. Mn or MnFe enrichment at 26°C seemed to increase the oxidative stress in zooxanthellae, since high LPO and glutathione reductase (GR) levels were recorded, but it did not cause any effect on polyp Hsp expression, probably due to the antioxidant action of GR. With the temperature increase, Mn enrichments prevented any increase in Hsp levels and caused a significant decrease of LPO and GR activity, strengthening a previous hypothesis suggesting that Mn could mitigate the negative cellular effects produced by the thermal stress.

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“…Oxidative stress is defined as an imbalance in the pro-oxidant/antioxidant ratio, which favors increased pro-oxidants and results in oxidative damage ( Downs et al, 2002 ; Halliwell and Gutteridge, 2007 ). Previous studies have shown that the elevated temperature and exposure to Cu are typically known to induce oxidative damage in M. harttii ( Fonseca et al, 2017 ; Marangoni et al, 2017 , 2019a , b ; Fonseca et al, 2021 ), as well as in other coral species ( Lesser, 1997 ; Schwarz et al, 2013 ; Dias et al, 2019 ). Given the clear connection between oxidative stress and coral bleaching (for a review see Suggett and Smith, 2019 ), it is paramount to evaluate changes in the activity of specific antioxidant molecules that are associated with this condition.…”

Section: Discussionmentioning

confidence: 99%

Elevated Temperature and Exposure to Copper Leads to Changes in the Antioxidant Defense System of the Reef-Building Coral Mussismilia harttii

et al. 2021

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The frequency and severity of coral bleaching events have increased in recent years. Global warming and contamination are primarily responsible for triggering these responses in corals. Thus, the objective of this study was to evaluate the isolated and combined effects of elevated temperature and exposure to copper (Cu) on responses of the antioxidant defense system of coral Mussismilia harttii. In a marine mesocosm, fragments of the coral were exposed to three temperatures (25.0, 26.6, and 27.3°C) and three concentrations of Cu (2.9, 5.4, and 8.6 μg/L) for up to 12 days. Levels of reduced glutathione (GSH) and the activity of enzymes, such as superoxide dismutase (SOD), catalase (CAT), glutathione S-transferase (GST), and glutamate cysteine ligase (GCL), were evaluated on the corals and symbionts. The short exposure to isolated and combined stressors caused a reduction in GSH levels and inhibition of the activity of antioxidant enzymes. After prolonged exposure, the combination of stressors continued to reduce GSH levels and SOD, CAT, and GCL activity in symbionts and GST activity in host corals. GCL activity was the parameter most affected by stressors, remaining inhibited after 12-days exposure. Interesting that long-term exposure to stressors stimulated antioxidant defense proteins in M. harttii, demonstrating a counteracting response that may beneficiate the oxidative state. These results, combined with other studies already published suggest that the antioxidant system should be further studied in order to understand the mechanisms of tolerance of South Atlantic reefs.

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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)

Cited by 23 publications

References 44 publications

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

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

Manganese Benefits Heat-Stressed Corals at the Cellular Level

Elevated Temperature and Exposure to Copper Leads to Changes in the Antioxidant Defense System of the Reef-Building Coral Mussismilia harttii

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