Microbes support enhanced nitrogen requirements of coral holobionts in a high CO 2 environment

Ocean acidification is posing a threat to calcifying organisms due to the increased energy requirements of calcification under high CO2 conditions. The ability of scleractinian corals to cope with future ocean conditions will thus depend on their ability to fulfil their carbon requirement. However, the primary productivity of coral holobionts is limited by low nitrogen (N) availability in coral reef waters. Here, we employed CO2 seeps of Tutum Bay (Papua New Guinea) as a natural laboratory to understand how coral holobionts offset their increased energy requirements under high CO2 conditions. Our results demonstrate for the first time that under high pCO2 conditions, N assimilation pathways of Pocillopora damicornis are jointly modified. We found that diazotroph-derived N assimilation rates in the Symbiodiniaceae were significantly higher in comparison to an ambient CO2 control site, concomitant with a restructured diazotroph community and the specific prevalence of an alpha-proteobacterium. Further, corals at the high CO2 site also had increased feeding rates on picoplankton and in particular exhibited selective feeding on Synechococcus sp., known to be rich in N. Given the high abundance of picoplankton in oligotrophic waters at large, our results suggest that corals exhibiting flexible diazotrophic communities and capable of exploiting N-rich picoplankton sources to offset their increased N requirements may be able to cope better in a high pCO2 world.

Autotrophic and heterotrophic nutrient fluxes in the dinoflagellate-coral symbiosis – A NanoSIMS perspective

Julia Marie Jeanne Yvonne Bodin, Isabelle Domart-Coulon, Maoz Fine, Thomas Krüger, Anders Meibom

The exchange of metabolites between photosynthetic symbionts and their coral host in shallow-water scleractinians provides the nutritional basis for their successful evolution and the existence of massive coral reefs in oligotrophic tropical waters. Autotrophic nutrition, based on carbon- and nitrogen-rich photosynthetic metabolites, is complemented by heterotrophic uptake and assimilation of organic matter to obtain additional carbon, nitrogen and phosphorus. By combining TEM ultrastructural observations with quantitative NanoSIMS isotopic imaging of tissue sections at sub-cellular resolution, we have compared the exchange of nutrients from the autotrophic assimilation of 15N-nitrate and 13C-bicarbonate with the heterotrophic uptake from 15N- and 13C-labelled brine shrimps in Stylophora pistillata from the Red Sea. Our results confirm that heterotrophy serves as the dominant source of nitrogen for the coral holobiont. On a time scale of 6 hours, heterotrophy provided approximately nine times more nitrogen to the host gastrodermal anabolism than symbiont nitrate fixation and translocation. Heterotrophic nitrogen was also used in anabolic processes in the symbionts, but at a level about 40% lower compared with nitrogen incorporation from nitrate fixation. The role of photosynthesizing symbionts the major contributors of carbon to the coral host was evident from the observation that autotrophic carbon enrichment in the gastrodermal layer was seven times higher in comparison to the heterotrophic carbon acquisition. Our observations directly demonstrate the complementing roles of heterotrophic and autotrophic food acquisition and support the notion that recycling of nutrients in symbiotic coral holobionts is critical to their vitality. The effects of stress from environmental change, including increasing water temperature and ocean acidification, are under investigation.

2015

Highly Variable and Non-complex Diazotroph Communities in Corals From Ambient and High CO2 Environments

Nils Rädecker

The ecological success of corals depends on their association with microalgae and a diverse bacterial assemblage. Ocean acidification (OA), among other stressors, threatens to impair host-microbial metabolic interactions that underlie coral holobiont functioning. Volcanic CO2 seeps offer a unique opportunity to study the effects of OA in natural reef settings and provide insight into the long-term adaptations under a low pH environment. Here we compared nitrogen-fixing bacteria (diazotrophs) associated with four coral species (Pocillopora damicornis, Galaxea fascicularis, Acropora secale, and Porites rus) collected from CO2 seeps at Tutum Bay (Papua New Guinea) with those from a nearby ambient CO2 site using nifH amplicon sequencing to characterize the effects of seawater pH on bacterial communities and nitrogen cycling. Diazotroph communities were of generally low diversity across all coral species and for both sampling sites. Out of a total of 25 identified diazotroph taxa, 14 were associated with P. damicornis, of which 9 were shared across coral species. None of the diazotroph taxa, however, were consistently found across all coral species or across all samples within a species pointing to a high degree of diazotroph community variability. Rather, the majority of sampled colonies were dominated by one or two diazotroph taxa of high relative abundance. Pocillopora damicornis and Galaxea fascicularis that were sampled in both environments showed contrasting community assemblages between sites. In P. damicornis, Gammaproteobacteria and Cyanobacteria were prevalent under ambient pCO(2), while a single member of the family Rhodobacteraceae was present at high relative abundance at the high pCO(2) site. Conversely, in G. fascicularis diazotroph communities were indifferent between both sites. Diazotroph community changes in response to OA seem thus variable within as well as between host species, potentially arguing for haphazard diazotroph community assembly. This warrants further research into the underlying factors structuring diazotroph community assemblages and their functional role in the coral holobiont.

FRONTIERS MEDIA SA2021

Subcellular Investigation of Photosynthesis-Driven Carbon and Nitrogen Assimilation and utilization in the Symbiotic Reef Coral: Pocillopora damicornis

Isabelle Domart-Coulon, Stéphane Laurent Escrig, Christophe Kopp, Anders Meibom

UNLABELLED: Reef-building corals form essential, mutualistic endosymbiotic associations with photosynthetic Symbiodinium dinoflagellates, providing their animal host partner with photosynthetically derived nutrients that allow the coral to thrive in oligotrophic waters. However, little is known about the dynamics of these nutritional interactions at the (sub)cellular level. Here, we visualize with submicrometer spatial resolution the carbon and nitrogen fluxes in the intact coral-dinoflagellate association from the reef coral Pocillopora damicornis by combining nanoscale secondary ion mass spectrometry (NanoSIMS) and transmission electron microscopy with pulse-chase isotopic labeling using [(13)C]bicarbonate and [(15)N]nitrate. This allows us to observe that (i) through light-driven photosynthesis, dinoflagellates rapidly assimilate inorganic bicarbonate and nitrate, temporarily storing carbon within lipid droplets and starch granules for remobilization in nighttime, along with carbon and nitrogen incorporation into other subcellular compartments for dinoflagellate growth and maintenance, (ii) carbon-containing photosynthates are translocated to all four coral tissue layers, where they accumulate after only 15 min in coral lipid droplets from the oral gastroderm and within 6 h in glycogen granules from the oral epiderm, and (iii) the translocation of nitrogen-containing photosynthates is delayed by 3 h.IMPORTANCE: Our results provide detailed in situ subcellular visualization of the fate of photosynthesis-derived carbon and nitrogen in the coral-dinoflagellate endosymbiosis. We directly demonstrate that lipid droplets and glycogen granules in the coral tissue are sinks for translocated carbon photosynthates by dinoflagellates and confirm their key role in the trophic interactions within the coral-dinoflagellate association.

American Society for Microbiology2015