Relative Diazotroph Abundance in Symbiotic Red Sea Corals Decreases With Water Depth

Abstract

Microbial dinitrogen (N 2) fixation (diazotrophy) is a trait critical for coral holobiont functioning. The contribution of N 2 fixation to holobiont nitrogen (N) supply likely depends on the ecological niche of the coral holobiont. Consequently, coral-associated diazotroph communities may exhibit distinct activity patterns across a water depth gradient. We thus compared relative abundances of diazotrophs in the tissues of two common hard coral species, Podabacia sp. and Pachyseris speciosa, along their water depth distribution (10-30 m and 30-50 m, respectively) in the Central Red Sea. The relative gene copy numbers of the nifH gene (i.e., referenced against the eubacterial 16S rRNA gene), as a proxy for N 2 fixation potential, were assessed via quantitative PCR. We hypothesized that relative nifH gene copy numbers would decrease with water depth, assuming a related shift from autotrophy to heterotrophy. Findings confirmed this hypothesis and revealed that nifH gene abundances for both corals decreased by ∼97% and ∼90% from the shallowest to the deepest collection site. However, this result was not significant for Pachyseris speciosa due to high biological variability. The observed decrease in nifH gene abundances may be explained by the relative increase in heterotrophy of the coral animal at increasing water depths. Our results underline the importance of interpreting microbial functions and associated nutrient cycling processes within the holobiont in relation to water depth range reflecting steep environmental gradients.

Diazotroph-Derived Nitrogen Assimilation Strategies Differ by Scleractinian Coral Species

“…It should be noted that in the present study, N 2 fixation rates by symbiotic diazotrophs were obtained at night, and are therefore maybe slightly lower than rates measured during the day. Bednarz et al (2017Bednarz et al ( , 2018, as well as Tilstra et al (2019), found that the ecological dependence of corals on diazotrophy might depend on depth, and so on light availability, with a decrease in relative nifH gene copy numbers with increasing depth. This may be linked to reduce photosynthate translocation by Symbiodiniaceae to the coral host, thus decreasing the fueling of the energy-expensive activity of coral-associated diazotrophs (Pogoreutz et al, 2017a).…”

“…Hence, when corals feed on plankton, it can ingest both planktonic diazotrophs, but also plankton that developed on DDN from planktonic diazotrophs (for simplicity, this pathway will be called hereafter "heterotrophic nutrition on diazotrophs"). Finally, symbiotic diazotrophs located in the coral tissue, coral mucus layer and skeleton, have the molecular machinery to fix N 2 (Lema et al, 2012;Bednarz et al, 2019) and this pathway has been evidenced as a N source in several corals species (Santos et al, 2014;Cardini et al, 2015;Tilstra et al, 2019). While recent works have shown that N acquisition through symbiotic N 2 fixation greatly varies in relation to environmental factors, species, but also corals' metabolic status (Rädecker et al, 2015;Bednarz et al, 2017;Benavides et al, 2017;Lesser et al, 2018Lesser et al, , 2019, heterotrophic nutrition on diazotrophs has only been demonstrated for one coral species, Stylophora pistillata in Benavides et al (2016) and Meunier et al (2019).…”

Microbes support enhanced nitrogen requirements of coral holobionts in a high CO2 environment

“…Finally, symbiotic diazotrophs, located in the animal tissue, coral mucus layer and skeleton, have the enzymatic machinery to fix atmospheric dinitrogen (N 2 ) and convert it into NH 4 + (Bednarz et al, 2019; Lema et al, 2012). This diazotroph‐derived N (DDN) has been recognized as an important alternative N source to compensate for dynamic fluctuations in environmental N availability (Cardini et al, 2015; Santos et al, 2014; Tilstra et al, 2019). Labelled 15 N 2 gas allows us to measure net N 2 fixation directly, and to trace the fate of DDN within the different coral compartments (Bednarz et al, 2017; Benavides et al, 2016; Meunier et al, 2019).…”

Relative abundance of nitrogen cycling microbes in coral holobionts reflects environmental nitrate availability

“…Quantitative PCRs (qPCRs) were carried out according to Tilstra et al [ 21 ]. Briefly, relative copy numbers of the functional genes nirS and nifH were used as a proxy for denitrification and diazotrophy, respectively, as implemented previously [ 20 , 21 , 30 ]. qPCR assays were performed in technical triplicates for each biological replicate (i.e.…”