Unravelling the Importance of Diazotrophy in Corals – Combined Assessment of Nitrogen Assimilation, Diazotrophic Community and Natural Stable Isotope Signatures

Abstract

There is an increasing interest in understanding the structure and function of the microbiota associated with marine and terrestrial organisms, because it can play a major role in host nutrition and resistance to environmental stress. Reef-building corals live in association with diazotrophs, which are microbes able to fix dinitrogen. Corals are known to assimilate diazotrophically-derived nitrogen (DDN), but it is still not clear whether this nitrogen source is derived from coral-associated diazotrophs and whether it substantially contributes to the coral’s nitrogen budget. In this study, we aimed to provide a better understanding of the importance of DDN for corals using a holistic approach by simultaneously assessing DDN assimilation rates (using 15N2 tracer technique), the diazotrophic bacterial community (using nifH gene amplicon sequencing) and the natural δ15N signature in Stylophora pistillata corals from the Northern Red Sea along a depth gradient in winter and summer. Overall, our results show a discrepancy between the three parameters. DDN was assimilated by the coral holobiont during winter only, with an increased assimilation with depth. Assimilation rates were, however, not linked to the presence of coral-associated diazotrophs, suggesting that the presence of nifH genes does not necessarily imply functionality. It also suggests that DDN assimilation was independent from coral-associated diazotrophs and may instead result from nitrogen derived from planktonic diazotrophs. In addition, the δ15N signature presented negative values in almost all coral samples in both seasons, suggesting that nitrogen sources other than DDN contribute to the nitrogen budget of corals from this region. This study yields novel insight into the origin and importance of diazotrophy for scleractinian corals from the Northern Red Sea using multiple proxies.

Metagenomic shifts in mucus, tissue and skeleton of the coral Balanophyllia europaea living along a natural CO2 gradient

“…Accordingly, the appearance of a regulatory protein of arginine utilization in coral mucus growing in acidified sites supports our hypothesis, since arginine is a building block for cyanophycin [ 107 ]. On the contrary, N fixation did not show acidification-related modifications in the involved genetic functions, in our Mediterranean coral model, confirming the importance of this pathway for coral survival pointed out by previous studies using 15 N 2 tracer technique [ 108 ]. Growth and density of Symbiodiniaceae algal symbiont within the coral host is highly dependent on N availability, and N fixation performed by bacteria could contribute to the stability of the coral–algae symbiosis, in particular under sub-optimal scenarios [ 109 ].…”

Symbiodiniaceae Are the First Site of Heterotrophic Nitrogen Assimilation in Reef-Building Corals

“…Reef samples also had lower δ 15 N-AAs than all aquarium treatments. Such a low isotopic ratio in corals from the Red Sea has been demonstrated previously ( 48 , 49 ). It is probably due to nitrate with low δ 15 N values entering the Red Sea system in the form of aerosols ( 48 , 50 ).…”

“…Such a low isotopic ratio in corals from the Red Sea has been demonstrated previously ( 48 , 49 ). It is probably due to nitrate with low δ 15 N values entering the Red Sea system in the form of aerosols ( 48 , 50 ). The above observations suggest that δ 13 C and δ 15 N-AAs of coral tissue must be combined with plankton abundance and environmental data before they can be used as reliable proxies for heterotrophy.…”

Desert dust deposition supplies essential bioelements to Red Sea corals

“…However, at low doses, such as those supplied by the dust (75 nM in this experiment), nitrate is a fundamental element for coral health, supplying sufficient nitrogen to oligotrophic reef waters to enhance or maintain coral metabolism without disrupting the symbiosis (Ezzat et al, 2019). The very low δ 15 N signatures of plankton (Kürten et al, 2016) and coral tissue (Alamaru et al, 2009; Bednarz et al, 2021) indeed suggest a significant supply of dust‐derived nitrate to the reef organisms (Wankel et al, 2010). In our study, however, there was no change in the δ 15 N signature of the dust‐exposed corals compared to control corals, nor in their elemental nitrogen content (Figure S2), likely due to the relatively short‐time exposure to dust compared to the coral tissue renewal time.…”