Nitrogen fixation by symbiotic cyanobacteria provides a source of nitrogen for the scleractinian coral Montastraea cavernosa

Abstract

Colonies of the Caribbean coral Montastraea cavernosa (Linnaeus) that harbor endosymbiotic cyanobacteria can fix nitrogen, whereas conspecifics without these symbionts cannot. The pattern of nitrogen fixation is diurnal and maximum rates occur in the early morning and evening. An analysis of delta N-15 stable isotope data showed that the zooxanthellae, but not the animal tissue, from colonies with cyanobacteria preferentially use the products derived from nitrogen fixation, and that these zooxanthellae also have a greater DNA content per cell, suggesting that these cells are in the DNA synthesis (S) and gap (G(2)) + Mitosis (M) phase of their cell cyle and are preparing to undergo cell division. Since nitrogen fixation did not occur during those times of the day when hyperoxia is known to occur, low oxygen concentrations might be required to support cyanobacterial respiration and provide the energy needed to fix nitrogen because the reaction centers of these cyanobacteria are uncoupled from light harvesting accessory pigments and the photosynthetic electron transport chain. Consistent with this were the depleted delta C-13 stable isotope signatures in all compartments of those corals with symbiotic cyanobacteria, which show an increase in heterotrophy compared with samples of M. cavernosa without cyanobacteria. Using modeled underwater light fields and measurements of photosynthesis, we show that the amount of time in which nitrogen fixation in these corals can take place increases with depth and that the distribution of corals with symbiotic cyanobacteria is positively correlated with increasing depth. The results presented here show that the zooxanthellae of M. cavernosa acquire nitrogen from cyanobacterial nitrogen fixation. Given that nitrogen limitation has long been proposed to contribute to the stability of these symbiotic associations, the mechanism by which zooxanthellae symbiosis in these corals is maintained remains an important question and the subject of future study.