Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates

Abstract

The 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 15 N. 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 15 N (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, F 5,53 = 18.03, P = 0.004 for Alteromonas sp. and F 5,53 = 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.

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

“…Both horizontal (environmental) and vertical (genetic) transmission has been reported for zooxanthellae and prokaryotic associates (Harrison and Wallace, 1990;Chen et al, 2010;Ceh et al, 2013b). If one or the other transmission predominates may depend -at least to some degree-on the reproduction strategy of the coral species under study, i.e., brooding vs. broadcasting corals (Apprill et al, 2009;Littman et al, 2009a;Ceh et al, 2013a). Prokaryotes could offer diverse metabolic functions to the coral holobiont, and hence it is plausible that they are mostly acquired horizontally triggered by nutritional needs or environmental stress situations , which is supported by the fact that horizontal transmission of bacteria often entails chemotaxis (Chen et al, 2010;Tout et al, 2015) and quorum sensing (Ransome et al, 2013).…”

“…It has been shown that adult corals release bacteria with their offspring and that coral larvae actively take up these bacteria into their tissue (Apprill et al, 2009;Ceh et al, 2013a,b). Roseobacter, Alteromonas and Vibrio-affiliated species are the most abundant bacterial taxa released by adult corals and are known to be capable of N 2 fixation (Ceh et al, 2013a). Using fluorescence in situ hybridization (FISH) and nanoSIMS the incorporation of Vibrio sp.…”

Responses of Coral-Associated Bacterial Communities to Local and Global Stressors

“…For example, diazotrophs (i.e., nitrogen-fixing microbes) form speciesspecific associations with corals and may provide limiting fixed nitrogen to the algal partner of corals, Symbiodinium, and to the coral animal itself (Lesser et al, 2004(Lesser et al, , 2007Lema et al, 2012). In the early coral life stages, bacteria provide nitrogen directly to larvae's Symbiodinium (Ceh et al, 2013a) and potentially to the coral larvae (Lema et al, 2014). Bacteria also play an important role in larval recruitment and settlement, for example, Alphaproteobacterium, Roseivivax sp.…”

Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora

“…and Alteromonas sp.) into coral larval tissues and associated Symbiodinium cells within 8 h of coral-bacterial incubations (Ceh et al, 2013). Although the latter demonstrated incorporation of labelled nitrogen from bacteria into coral and Symbiodinium cells, the presence of these bacteria in coral host tissues could not be confirmed and the capacity of these bacteria to fix dinitrogen gas was not investigated.…”