Evidence for mitigation of coral bleaching by manganese

Abstract

Unprecedented mass coral bleaching events due to global warming and overall seawater pollution have been observed worldwide over the last decades. Although metals are often considered as toxic substances for corals, some are essential at nanomolar concentrations for physiological processes such as photosynthesis and antioxidant defenses. This study was designed to elucidate, the individual and combined effects of nanomolar seawater enrichment in manganese (Mn) and iron (Fe), on the main physiological traits of Stylophora pistillata, maintained under normal growth and thermal stress conditions. We provide, for the first time, evidence that Mn is a key trace element for coral symbionts, enhancing cellular chlorophyll concentrations, photosynthetic efficiency and gross photosynthetic rates at ambient temperature. Our experiment also highlights the key role of Mn in increasing coral resistance to heat stress-induced bleaching. While Mn-enriched corals did not bleach and did not reduce their rates of photosynthesis and calcification, control corals experienced significant bleaching. On the contrary to Mn, Fe enrichment not only impaired calcification but induced significant bleaching. Such information is an important step towards a better understanding of the response of corals to seawater enrichment in metals. It can also explain, to some extent, species susceptibility to environmental stress.

Determinants of Tubastraea coccinea invasion and likelihood of further expansion in the northern Gulf of Mexico

“…Although phytoplankton are eaten by zooplankton, which in turn are eaten by T. coccinea, corals prefer oligotrophic waters, where primary productivity is low (Sheppard et al 2017;Martin 2018). Also, iron enrichment can lead to impaired calcification and significant bleaching in corals (Biscéré et al 2018). These factors might explain T. coccinea's presence being associated with low minimum iron levels.…”

Coral bleaching patterns are the outcome of complex biological and environmental networking

“…Over three decades of experiments and observations have developed and refined the central bleaching paradigm (e.g., Cziesielski et al, ) whereby accumulation of reactive oxygen species (ROS), and/or reactive nitrogen species (RNS), leads to signaling cascades and in turn expulsion or xenophagy of the algal endosymbionts (Family: Symbiodiniaceae) from the coral host (Davy et al, ; Smith et al, ; Tchernov et al, ; Weis, ). An overwhelming body of evidence has repeatedly demonstrated that perturbations to environmental factors underpinning optimum metabolic functioning can all result in bleaching; notably, temperature (Levin et al, ; Tchernov et al, ; Tolleter et al, ), light (Downs et al, ; Lesser & Farrell, ), salinity (Aquilar et al, 2019; Gardner et al, ; Ochsenkühn, Röthig, D'Angelo, Wiedenmann, & Voolstra, ) as well as inorganic nutrients including CO 2 (Anthony, Kline, Diaz‐Pulido, Dove, & Hoegh‐Guldberg, ; Crawley et al, ), iron and other trace metals (Biscéré, Ferrier‐Pagès, Gilbert, Pichler, & Houlbrèque, ; Ferrier‐Pagès et al, ; Shick et al, ), and the nitrogen‐to‐phosphate ratio (Fabricius, Cséke, Humphrey, & De'ath, ; Pogoreutz et al, ; Wiedenmann et al, ). Stability of the symbiosis rests on fine‐tuned resource exchange of primary metabolic currencies—C, N, P, electron carriers, etc.—among the algal symbionts, host, and/or broader associated microbiome (Suggett, Warner, & Leggat, ).…”

Manganese Benefits Heat-Stressed Corals at the Cellular Level

“…In this regard, an increased bleaching susceptibility of scleractinian corals has been observed when subjected to the combined effects of thermal stress and copper or nickel enrichment (Biscéré et al, 2017;Fonseca et al, 2017;Banc-Prandi and Fine, 2019). Also, iron enrichment has been shown to impair calcification and induce significant bleaching (Wells et al, 2011;Biscéré et al, 2018). On the contrary, manganese enrichment may alleviate the deleterious effect of heat stress on corals, by enhancing chlorophyll concentrations, photosynthetic efficiency, and gross photosynthetic rates at ambient and elevated temperature (Biscéré et al, 2018).…”

“…Also, iron enrichment has been shown to impair calcification and induce significant bleaching (Wells et al, 2011;Biscéré et al, 2018). On the contrary, manganese enrichment may alleviate the deleterious effect of heat stress on corals, by enhancing chlorophyll concentrations, photosynthetic efficiency, and gross photosynthetic rates at ambient and elevated temperature (Biscéré et al, 2018). All together, these studies suggest that the effects of metals on coral physiology are metal and concentration-dependent, and that interactions between metals also exist.…”

“…A previous work dealing with the effect of manganese and/or iron enrichment in combination with thermal stress has shown interesting results on coral physiology, particularly with reference to the potential role of manganese in the reduction of heat stress impact, likely due to its involvement in the antioxidant system (Biscéré et al, 2018). Starting from these statements, we performed on the same coral samples an in-depth analysis of the cellular mechanisms underlying the response observed by Biscéré et al (2018), in order to better understand the role of manganese and iron, which is poorly elucidated when compared to that of other metals (Schwarz et al, 2013;Biscéré et al, 2017;Bielmyer-Fraser et al, 2018;Zhou et al, 2018;Marangoni et al, 2019c). In particular, in this study we analyzed the individual and combined effects of prolonged heat stress and metal enrichment (Mn and Fe) at the cellular level on the coral Stylophora pistillata, by investigating changes in the host cellular protein homeostasis, and the holobiont oxidative status.…”