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Dissolved Nitrogen Acquisition in The Dissolved Nitrogen Acquisition in the Symbioses of Soft and Hard Corals With Symbiodiniaceae: A Key to Understanding Their Different Nutritional Strategies? Chloé Pupier, Renaud Grover, Maoz Fine, Cécile Rottier, Jeroen van de Water, Christine Ferrier-Pagès To cite this version: Chloé Pupier, Renaud Grover, Maoz Fine, Cécile Rottier, Jeroen van de Water, et al.. Dissolved Nitrogen Acquisition in the Symbioses of Soft and Hard Corals With Symbiodiniaceae: A Key to Understanding Their Different Nutritional Strategies?. Frontiers in Microbiology, Frontiers Media, 2021, 12, pp.657759. 10.3389/fmicb.2021.657759. hal-03268546 HAL Id: hal-03268546 https://hal.sorbonne-universite.fr/hal-03268546 Submitted on 23 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. fmicb-12-657759 May 28, 2021 Time: 17:29 # 1 ORIGINAL RESEARCH published: 04 June 2021 doi: 10.3389/fmicb.2021.657759 Dissolved Nitrogen Acquisition in the Symbioses of Soft and Hard Corals With Symbiodiniaceae: A Key to Understanding Their Different Nutritional Strategies? Chloé A. Pupier1,2*, Renaud Grover1, Maoz Fine3,4, Cécile Rottier1, Jeroen A. J. M. van de Water1 and Christine Ferrier-Pagès1 1 Marine Department, Centre Scientifique de Monaco, Monaco, Monaco, 2 Collège Doctoral, Sorbonne Université, Paris, France, 3 The Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat Gan, Israel, 4 The Interuniversity Institute for Marine Science in Eilat, Eilat, Israel Edited by: Nitrogen is one of the limiting nutrients for coral growth and primary productivity. Zhiyong Li, Therefore, the capacity of different associations between corals and their algal Shanghai Jiao Tong University, China symbionts (Symbiodiniaceae) to efficiently exploit the available nitrogen sources Reviewed by: Shan-Hua Yang, will influence their distribution and abundance. Recent studies have advanced our National Taiwan University, Taiwan understanding of nitrogen assimilation in reef-building scleractinian (hard) coral- Diogo Antonio Tschoeke, Federal University of Rio de Janeiro, Symbiodiniaceae symbioses. However, the nutrient metabolism of other coral taxa, Brazil such as Alcyoniina (soft corals), remains underexplored. Using stable isotope labeling, *Correspondence: we investigated the assimilation of dissolved nitrogen (i.e., ammonium, nitrate, and free Chloé A. Pupier amino acids) by multiple species of soft and hard corals sampled in the Gulf of Aqaba [email protected] in shallow (8–10 m) and mesophotic (40–50 m) reefs. Our results show that dissolved Specialty section: nitrogen assimilation rates per tissue biomass were up to 10-fold higher in hard than in This article was submitted to soft coral symbioses for all sources of nitrogen. Although such differences in assimilation Microbial Symbioses, a section of the journal rates could be linked to the Symbiodiniaceae density, Symbiodiniaceae species, or the Frontiers in Microbiology C:N ratio of the host and algal symbiont fractions, none of these parameters were Received: 23 January 2021 different between the two coral taxa. Instead, the lower assimilation rates in soft coral Accepted: 23 April 2021 Published: 04 June 2021 symbioses might be explained by their different nutritional strategy: whereas soft corals Citation: may obtain most of their nitrogen via the capture of planktonic prey by the coral host Pupier CA, Grover R, Fine M, (heterotrophic feeding), hard corals may rely more on dissolved nitrogen assimilation Rottier C, van de Water JAJM and by their algal symbionts to fulfill their needs. This study highlights different nutritional Ferrier-Pagès C (2021) Dissolved Nitrogen Acquisition in the Symbioses strategies in soft and hard coral symbioses. A higher reliance on heterotrophy may help of Soft and Hard Corals With soft corals to grow in reefs with higher turbidity, which have a high concentration of Symbiodiniaceae: A Key to Understanding Their Different particles in suspension in seawater. Further, soft corals may benefit from lower dissolved Nutritional Strategies? nitrogen assimilation rates in areas with low water quality. Front. Microbiol. 12:657759. doi: 10.3389/fmicb.2021.657759 Keywords: nitrogen, nutrition, octocoral, mesophotic, stable isotopes Frontiers in Microbiology| www.frontiersin.org 1 June 2021| Volume 12| Article 657759 fmicb-12-657759 May 28, 2021 Time: 17:29 # 2 Pupier et al. Dissolved Nitrogen Acquisition in Corals INTRODUCTION taxa such as soft corals (sub-order Alcyoniina) have been largely overlooked (Schlichter, 1982; Burris, 1983), despite being the Nitrogen (N) is essential for the life and growth of all organisms second most common benthic group on many reefs and therefore on Earth, as it is required for the biosynthesis of key cellular recognized as key taxa (Schubert et al., 2017). The lack of data components. However, N is a growth-limiting nutrient in on soft corals, along with the use of different data normalization oligotrophic marine ecosystems, such as coral reefs (de Goeij metrics in studies on soft and hard corals, limit our ability to et al., 2013). Corals are the primary reef-building and habitat- predict how nutrient conditions may favor the growth of one forming species in these marine environments and require a group over the other. High abundances of octocorals (soft corals steady supply of nutrients for growth and reproduction. As a or gorgonians) have, however, been observed on eutrophicated consequence, they have evolved as meta-organisms or holobionts reefs, where high concentrations of nutrients in the water do (Rohwer et al., 2002; Bosch and McFall-Ngai, 2011), in which the not favor the growth of hard corals (Bell, 1992; Gast et al., 1999; host is associated with an assemblage of microorganisms. These Baum et al., 2016; Vollstedt et al., 2020). This dominance of microbial communities are notably involved in the protection soft corals in disturbed reef ecosystems suggests that they may against pathogens and in the efficient uptake and recycling of the have a different nutrient metabolism or nutritional relationship few available nutrients (Rädecker et al., 2015). with their symbionts compared with hard corals. Also, corals The coral animal itself is mainly capable of assimilating tend to increase their reliance on heterotrophy with depth particulate and dissolved organic N [e.g., dissolved free amino (mesophotic reefs), although this might be species-dependent acids (DFAA) and urea] (Grover et al., 2006, 2008). However, (Muscatine and Kaplan, 1994). microbes involved in all steps of the N cycle have been found in To gain better insights into the extent to which soft corals the microbiota of corals. For example, N-fixing microorganisms rely on their symbionts for their nutrition, we investigated how (Benavides et al., 2017) convert N2 gas into bioavailable these symbiotic associations assimilate different DN forms, C ammonium (NH4 ), and numerous microbes, including the and how this may be impacted by depth and temperature. common hard and soft coral symbiont Endozoicomonas, can We hypothesized (1) that Symbiodiniaceae in symbiosis − C perform dissimilatory nitrate (NO3 ) reduction into NH4 with soft corals can use all DN forms, and (2) that low (Neave et al., 2014). Finally, the algal symbionts belonging to the irradiance (as measured at mesophotic depths) or elevated family Symbiodiniaceae (LaJeunesse et al., 2018) are the main temperatures will negatively affect the assimilation rates of assimilation site of the dissolved inorganic N forms (DIN), such DN, as previously observed for hard corals. In addition, we C − as NH4 and NO3 (Muscatine et al., 1979; Grover et al., 2002, conducted a comparative study with hard corals, allowing a 2003; Pernice et al., 2012). better understanding of the differences in the functional and The assimilation of dissolved N (DN) by corals is, however, nutritional ecology of soft and hard corals, with the underlying influenced by both the environmental conditions and the algal hypothesis that soft corals rely less on the assimilation of DN symbionts they are associated with. For example, some genera than hard corals because they are generally considered as more of Symbiodiniaceae take up nutrients more efficiently than heterotrophic. A higher reliance on heterotrophy may help soft others (Baker A.C. et al., 2013; Leal et al., 2015; Pernice et al., corals to grow in reefs with high turbidity, and they may benefit 2015), and high light levels promote their DN assimilation from low DN assimilation rates in areas with low water quality. (Grover et al., 2008). In contrast, elevated seawater temperatures reduce DIN availability in surface waters due to enhanced water column stratification, which prevents the upwelling of MATERIALS AND METHODS nutrients recycled in deep waters (Behrenfeld et al., 2006). It also induces coral bleaching and thereby impairs the ability of Biological Material the remaining symbionts to take up DIN (Godinot et al., 2011; The study was conducted at the Inter-University Institute Krueger et al., 2018). (IUI) for Marine Sciences (Eilat, Israel)
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