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

Arjen Tilstra,Claudia Pogoreutz,Christian Wild,Christian R Voolstra,Maren Ziegler,Nils Rädecker

doi:10.3389/fmars.2019.00372

Abstract

Microbial dinitrogen (N2) fixation (diazotrophy) is a trait critical for coral holobiont functioning. The contribution of N2 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 proxy for N2 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.

Highlights

Scleractinian corals are associated with a diverse microbial community
The quantitative PCR (qPCR) results confirmed the presence of the nifH gene in the microbial communities associated with both investigated Red Sea coral species and across the entire distribution range of sampling depths (Figure 1)
Despite belonging to two different coral families (Fungiidae and Agariciidae) and exhibiting differences in water depth distribution range, the two coral species exhibited a similar pattern: relative nifH gene copy numbers for each coral species were highest at the two shallowest water depths and decreased at the greatest water depth (Figure 1)

Summary

INTRODUCTION

Scleractinian corals are associated with a diverse microbial community. This microbiome is comprised of dinoflagellate algae of the family Symbiodiniaceae (LaJeunesse et al, 2018) and a multitude of other eukaryotic and prokaryotic microbes that together form a meta-organism, the coral holobiont (Rohwer et al, 2002). As O2 availability within the coral tissues can exhibit considerable diurnal variation due to high rates of photosynthesis by Symbiodiniaceae during the day (Sorek et al, 2013), irradiance may be a critical driver of coral-associated N2 fixation (Bednarz et al, 2017). As heterotrophic food sources have a higher N content than photosynthate provided by Symbiodiniaceae, the N demand of the coral holobiont may decrease with increasing heterotrophy (Dubinsky and Jokiel, 1994) In this light, Pogoreutz et al (2017b) showed a negative correlation of N2 fixation activity with heterotrophic potential of scleractinian corals by using relative nifH gene copy numbers as a proxy for N2 fixation potential. To assess the relative abundance of diazotrophs in the coral microbiome, relative nifH gene copy numbers were obtained via quantitative PCR of the nifH gene normalized to the 16S rRNA gene (Pogoreutz et al, 2017a,b)

MATERIALS AND METHODS

RESULTS

DISCUSSION