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Houlbreque, F.; Meunier, V.; , .; Camps, M. Diazotrophs Makes Corals More Resistant to Heat Stress. Encyclopedia. Available online: https://encyclopedia.pub/entry/21907 (accessed on 22 July 2024).
Houlbreque F, Meunier V,  , Camps M. Diazotrophs Makes Corals More Resistant to Heat Stress. Encyclopedia. Available at: https://encyclopedia.pub/entry/21907. Accessed July 22, 2024.
Houlbreque, Fanny, Valentine Meunier,  , Mercedes Camps. "Diazotrophs Makes Corals More Resistant to Heat Stress" Encyclopedia, https://encyclopedia.pub/entry/21907 (accessed July 22, 2024).
Houlbreque, F., Meunier, V., , ., & Camps, M. (2022, April 19). Diazotrophs Makes Corals More Resistant to Heat Stress. In Encyclopedia. https://encyclopedia.pub/entry/21907
Houlbreque, Fanny, et al. "Diazotrophs Makes Corals More Resistant to Heat Stress." Encyclopedia. Web. 19 April, 2022.
Diazotrophs Makes Corals More Resistant to Heat Stress
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This entry is adapted from the peer-reviewed paper 10.3390/biom12040537

During bleaching, corals expel millions of their symbionts, depriving the host from its main food source. One mechanism used by corals to resist bleaching consists in exploiting food sources other than autotrophy. Among the food sources available in the reefs, dinitrogen (N2)-fixing prokaryotes or planktonic diazotrophs (hereafter called ‘PD’) have the particularity to reduce atmospheric dinitrogen (N2) and release part of this nitrogen (diazotroph-derived nitrogen or DDN) in bioavailable form. The supply of PD allowed corals to maintain minimal chlorophyll concentration and symbiont density, sustaining photosynthetic efficiency and stimulating coral growth of up to 48% compared to unfed ones. By providing an alternative source of bioavailable nitrogen and carbon, this specific planktonic diazotroph feeding may have a profound potential for coral bleaching recovery. 

coral heat stress coral bleaching heterotrophy diazotrophy climate change

1. Introduction

The success of scleractinian corals in nutrient-poor waters surrounding coral reefs is due to their symbiosis with unicellular dinoflagellates belonging to the Symbiodiniaceae family [1]. These symbionts translocate a large fraction of photosynthetically fixed carbon (C) and amino acids to the host for its nutritional needs [2]. Coral reefs are experiencing increasingly frequent and devastating bleaching events [3]. During bleaching, corals expel millions of their symbionts and/or suffer a loss of photosynthetic pigments, depriving the host from its main nutrition source [4][5]. This process leads to coral death and to the decline of coral reefs if bleached corals are not able to rapidly recover their symbionts [3]. Bleaching susceptibility varies among species, depths, and locations (e.g., [6][7][8][9]), and is also influenced by coral morphology [10][11], physiological responses of both animal and symbionts [12][13], and symbiont types hosted by corals (e.g., [14][15][16]).
Another mechanism used to resist and recover from bleaching consists in exploiting food sources other than autotrophy. Indeed, corals are voracious predators that can feed on a wide range of prey ranging from pico-nanoplanktonic cells (with a size < 20 µm; [17]) to macrozooplankton [18][19]. Multiple laboratory experiments have shown that heterotrophy increases skeletal and tissue growth [17][20][21][22][23], allows corals to build up energy reserves [24][25], increases fertility [26], and reduces sensitivity to acidification [27][28][29]. Coral ability to switch from an autotrophic to a heterotrophic diet by increasing their feeding rates on zooplankton [22][30][31], making them more resistant to bleaching [30][32][33][34], has been much less studied. Only two studies have shown that corals increase their consumption of pico-nanoplankton during heat stress [35][36]. Among these small preys, dinitrogen (N2)-fixing prokaryotes (subsequently referred to as planktonic diazotrophs, hereafter called ‘PD’) have received little attention. Many coral reef ecosystems are characterized by high planktonic diazotroph abundance and activity; they are very widespread in the Western South Pacific (e.g., New Caledonia, Papua New Guinea, and the Australian Great Barrier Reef) [37][38][39][40] but also in Hawaii, in the Caribbean, and the Red Sea [41][42][43]. In New Caledonia, planktonic diazotrophs support ~80% of the primary production of other phytoplankton in summer [44][45]. The lagoon is dominated by picoplankton (non-diazotrophic, i.e., Synechococcus and Prochlorococcus) but the diazotrophs, even if they are less abundant, are much larger (nanoplankton and microplankton size) and thus represent an important part of the total biomass [46]. Planktonic diazotrophs reduce atmospheric N2 into bioavailable ammonium (NH4+), and release part of the recently fixed nitrogen (Diazotroph-Derived Nitrogen, DDN) in seawater, providing sufficient nitrogen stocks for the development of the planktonic food web in oligotrophic waters [47]. These planktonic diazotroph cells are thus, by definition, very rich in nitrogen (N) [48][49]. Their ingestion by scleractinian corals was first demonstrated by [50] using the 15N2 labelling method. Direct consumption of planktonic diazotrophs would provide 0.76 ± 0.15 μg N cm−2 h−1 to corals, which corresponds to six times the daily N supply by non-diazotrophic pico- and nanoplankton [17]. Bleached colonies of Stylophora pistillata incorporate more PD than healthy colonies [36], but the consequences on coral metabolism are not known. By providing an alternative source of bioavailable N and C, this increased incorporation of PD may have a profound influence on coral bleaching recovery.
To improve the understanding of the physiological response of corals to heat stress in anticipation of more frequent and severe coral bleaching events, the researchers investigated if and how nutrition on PD is involved in the resistance to high temperature of the coral species S. pistillata. The researchers evaluated key physiological measurements (photosynthetic efficiency, growth rates) and tissue parameters (chlorophyll, protein concentrations, and symbiont densities) of colonies of S. pistillata, fed or not with PD during heat stress.

2. Current Insights

Some coral species are able to increase their heterotrophic nutrition during bleaching episodes, which supplies their energy reserves, providing them with greater resistance, improved chances of survival [25][30][34][51][52][53], and allows them to recover their symbionts [54][55]. These conclusions were drawn by focusing primarily on the ingestion of mesozooplankton, and no study had so far investigated smaller planktonic fractions. The researchers' experiment provides the first evidence that heat-stressed PD-fed corals are able to retain part of their symbionts and chlorophyll and appear more resistant compared to heat-stressed unfed ones, which died after only 8 days. The researchers also show that a supply in planktonic diazotrophs (particularly rich in N) also alleviates some of the negative effects of heat stress on coral growth and photosynthetic efficiency.
In ambient conditions, feeding on planktonic diazotrophs induced significant changes in most coral physiological parameters. After 9 weeks of a planktonic diazotrophs’ diet, colonies significantly increased their chlorophyll contents. Corals benefit from these planktonic diazotrophs, directly either by grazing them [36][50], and/or indirectly by uptaking the DIN (dissolved inorganic nitrogen: NH4+ and DON) they released in surrounding waters [49][56][57]. This stimulation of the symbiotic compartment has been highlighted before for mesozooplankton-fed corals (e.g., [20][58][59][60]). As heterotrophy results in a significant release of NH4+ and as this NH4+ accumulates 14 to 23 times faster in the Symbiodiniaceae than in animal cells [61][62][63], planktonic diazotrophs’ diet stimulated pigment synthesis and symbiont division. The richness of planktonic diazotroph cells in vitamin B12 [64], which is an essential nutrient for the coral holobiont [65], has also contributed to this stimulation of the symbiotic compartment. In the research, ETRmax and Fv/Fm values of fed corals were similar to those of the unfed ones, and not higher as it has been demonstrated in mesozooplankton-fed corals (e.g., [22][60]). The PD-fed corals having higher symbiont densities should result in higher photosynthetic rates per surface regardless [21][22][55][66]. Given the N richness of diazotrophic cells, this specific diet should modify the photosynthate quality, with the highest amounts of N-rich amino acids [67].
One of the major results of this research is that an exclusive nutritional diet of planktonic diazotrophs stimulated coral growth by 48% compared to the unfed corals. The researchers' data confirm that feeding enhances skeletal growth, suggesting that corals allocate a high proportion of the energy brought by planktonic diazotrophs to skeleton growth processes [59][68][69][70]. Skeleton growth is a dual process, involving the secretion of an organic matrix and the deposition of a CaCO3 fraction. The contribution of diazotrophic plankton, particularly rich in N, could thus participate in a stimulation of the production of this organic matrix, mainly composed of proteins, glycoproteins, and polysaccharides [71][72][73], as already demonstrated in mesozooplankton-fed corals [59]. This growth stimulation by planktonic diazotrophs could also be achieved indirectly by boosting photosynthesis as stated above. These two stimulating ways make that growth rates in fed corals, submitted to heat stress, remain stable and always higher than those of unfed ones in the same conditions. In [55], calcification rates of S. pistillata colonies fed for 9 weeks with Artemia salina were reduced by up to 65% compared to control temperatures. Unlike A. salina nauplii, planktonic diazotrophs release large amounts of NH4+ and DON into the surrounding water [49][56][57]. This surplus of N provided by the planktonic diazotrophs might have reduced calcification sensitivity to heat stress, as demonstrated for corals submitted to moderate nutrient inputs [74][75].
In corals under heat stress, the supply in planktonic diazotrophs helped maintain a minimal chlorophyll concentration and symbiont density to prevent a large decrease in the RLC curves, and above all, the colonies’ death. A decrease in chlorophyll content and symbiont densities was observed in heat-PD-fed corals (decrease of respectively 85% and 88%) but contrary to heat-unfed corals, all heat-PD-fed corals stayed alive, managed to keep some of their symbionts and pigments, and grew faster. As in the studies testing the effects of the ingestion of Artemia salina nauplii on the same species (S. pistillata; [21][22][76]), planktonic diazotrophs helped maintain photosynthetic efficiency of PSII. The input of this new N might have (i) facilitated the protein repair and re-synthesis of the PSII D1 protein (reviewed by [76][77]), (ii) increased the photosynthetic and photoprotective pigment (such as xanthophyll and peridinin) contents in coral tissue as in corals submitted to a moderate DIN enrichment [75], and/or (iii) reduced the degradation of the symbionts by increasing the synthesis of antioxidant compounds or heat-shock proteins [76][78].
These results clearly show a positive effect of planktonic diazotroph feeding under heat stress, sustaining photosynthetic efficiency and growth of S. pistillata colonies. So far, heterotrophic feeding on planktonic diazotrophs has been little considered compared to the N supply provided by coral-associated diazotrophs. However, in the case of heat stress, Ref. [79] have recently shown that this N supply by coral-associated diazotrophs is compromised. A 10-day heat stress caused a change in coral-associated diazotroph communities, which led to a 30% decrease in fixed N. Conversely, the researchers' previous works highlighted that N supply by planktonic diazotrophs (i) can fulfill a large part of the coral N requirements, compared to the symbiotic fixation ([50][53][80][81]) and (ii) is significant for several coral species [53]. This last research finally demonstrates that, contrary to endosymbiotic diazotrophs, a supply of planktonic diazotrophs allows corals to be more resistant to bleaching. It is therefore particularly essential to consider the contribution of DDN by planktonic diazotrophs in the coral holobiont N cycling which appears to be one of the main strategies for coral recovery facing bleaching. In the context of climate change, marine heat waves are becoming more intense and frequent and coral reefs are among the most vulnerable ecosystems to this emerging threat [82][83]. The researchers' very encouraging results imply that coral reefs where planktonic diazotrophs are abundant (e.g., Papua New Guinea, New Caledonia) could be more resistant to climate change. A supply of planktonic diazotrophs on the reefs could be included among innovative management approaches to improve the resilience of coral reefs with high conservation potential, during and after bleaching episodes [84][85].

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Fanny Houlbreque
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