Abstract

AbstractThe waters surrounding coral reef ecosystems are generally poor in nutrients, yet their levels of primary production are comparable with those reported from tropical rain forests. One explanation of this paradox is the efficient cycling of nutrients between the coral host, its endosymbiotic alga Symbiodinium and a wide array of microorganisms. Despite their importance for the animals' fitness, the cycling of nutrients in early coral life stages and the initial establishment of partnerships with the microbes involved in these processes has received little scrutiny to date. Nitrogen is an essential but limited nutrient in coral reef ecosystems. In order to assess the early nutrient exchange between bacteria and corals, coral larvae of the species Pocillopora damicornis were incubated with two coral‐associated bacteria (Alteromonas sp., or Vibrio alginolyticus), prelabeled with the stable nitrogen isotope 15N. The incorporation and translocation of nitrogen from Vibrio‐ and Alteromonas bacteria into P. damicornis coral larvae and specifically into the coral‐symbiotic Symbiodinium were detected by nanoscale secondary ion mass spectrometry (NanoSIMS). A significant increase in the amount of enriched 15N (two to threefold compared to natural abundance) was observed in P. damicornis larvae within 8 h of incubation for both bacterial treatments (one‐way ANOVA, F5,53 = 18.03, P = 0.004 for Alteromonas sp. and F5,53 = 18.03, P = 0.0001 for V. alginolyticus). These findings reveal that coral larvae acquire nutrients previously taken up from the environment by bacteria. The additional nitrogen may increase the survival rate and fitness of the developing coral and therefore contribute to the successful maintenance of coral reefs.

Highlights

  • Nitrogen is an essential element for life on Earth due to its requirement for cell maintenance, growth, and functioning

  • The mosaic of individual NanoSIMS images provided an overview of the location and distribution of 15N nitrogen enrichment through the cross section of a P. damicornis larva incubated with Alteromonas bacteria (Fig. 1). 15N hotspots were clearly evident in the coral symbiont Symbiodinium and in the outer ectodermis (Fig. 2)

  • Hotspots including the Symbiodinium, endodermis, and ectodermis tissues imaged in the P. damicornis larvae were further investigated with higher magnification and with longer counting times and the 15N/14N ratios were determined for the different tissue types after 8 and 24 h of incubation with each bacterial treatment (Fig. 3, Table S1). 15N levels increased significantly in larvae treated with Alteromonas sp. (15N Atom% 0.675, one-way ANOVA, F5,53=18.03, P = 0.004) and V. alginolyticus, (15N Atom% 0.861, F5,53 = 18.03, P = 0.0001) compared to controls within 8 h (15N Atom% 0.378)

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Summary

Introduction

Nitrogen is an essential element for life on Earth due to its requirement for cell maintenance, growth, and functioning. Bacteria convert inert atmospheric nitrogen into compounds such as ammonium that can be readily used by other organisms (Guerinot and Patriquin 1981; Lesser et al 2004, 2007; Taylor et al 2007). These coral reef symbiotic associations have coevolved and can influence the ecology of the host through nitrogen cycling processes like nitrogen fixation, nitrification, denitrification, and anaerobic ammonium oxidation (ANAMMOX)

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