Showing papers by "Anders Meibom published in 2015"

Subcellular Investigation of Photosynthesis-Driven Carbon Assimilation in the Symbiotic Reef Coral Pocillopora damicornis

Abstract: 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.

A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals

Abstract: Nutritional interactions between corals and symbiotic dinoflagellate algae lie at the heart of the structural foundation of coral reefs. Whilst the genetic diversity of Symbiodinium has attracted particular interest because of its contribution to the sensitivity of corals to environmental changes and bleaching (i.e. disruption of coral-dinoflagellate symbiosis), very little is known about the in hospite metabolic capabilities of different Symbiodinium types. Using a combination of stable isotopic labelling and nanoscale secondary ion mass spectrometry (NanoSIMS), we investigated the ability of the intact symbiosis between the reef-building coral Isopora palifera, and SymbiodiniumC or D types, to assimilate dissolved inorganic carbon (via photosynthesis) and nitrogen (as ammonium). Our results indicate that Symbiodinium types from two clades naturally associated with I.palifera possess different metabolic capabilities. The SymbiodiniumC type fixed and passed significantly more carbon and nitrogen to its coral host than the D type. This study provides further insights into the metabolic plasticity among different Symbiodinium types in hospite and strengthens the evidence that the more temperature-tolerant SymbiodiniumD type may be less metabolically beneficial for its coral host under non-stressful conditions.

Morphology, microstructure, crystallography, and chemistry of distinct CaCO3 deposits formed by early recruits of the scleractinian coral Pocillopora damicornis

Abstract: Scleractinian corals begin their biomineralization process shortly after larval settlement with the formation of calcium carbonate (CaCO(3)) structures at the interface between the larval tissues and the substrate. The newly settled larvae exert variable degrees of control over this skeleton formation, providing an opportunity to study a range of biocarbonate structures, some of which are transient and not observed in adult coral skeletons. Here we present a morphological, structural, crystallographic, and chemical comparison between two types of aragonite deposits observed during the skeletal development of 2-days old recruits of Pocillopora damicornis: (1) Primary septum and (2) Abundant, dumbbell-like structures, quasi-randomly distributed between initial deposits of the basal plate and not present in adult corals-At the mesoscale level, initial septa structures are formed by superimposed fan-shaped fasciculi consisting of bundles of fibers, as also observed in adult corals. This organization is not observed in the dumbbell-like structures. However, at the ultrastructural level there is great similarity between septa and dumbbell components. Both are composed of <100 nm granular units arranged into larger single-crystal domains.Chemically, a small difference is observed between the septae with an average Mg/Ca ratio around 11 mmol/mol and the dumbbell-like structures with ca. 7 mmol/mol; Sr/Ca ratios are similar in the two structures at around 8 mmol/mol-Overall, the observed differences in distribution, morphology, and chemistry between septa, which are highly conserved structures fundamental to the architecture of the skeleton, and the transient, dumbbell-like structures, suggest that the latter might be formed through less controlled biomineralization processes. Our observations emphasize the inherent difficulties involved in distinguishing different biomineralization pathways based on ultrastructural and crystallographical observations.

Feeding behaviour of a benthic species (Ammonia tepida) under oxic and anoxic conditions; TEM-NanoSIMS correlation

Abstract: More and more marine areas are subjected to depleted-O2 concentration, mainly due to eutrophication induced by human activities. These phenomena affect benthic ecosystems, in particular continental shelves and coastal areas where the renewal of the bottom waters is low and/or the organic matter flux is high. Some species of benthic foraminifera are resistant to this hypoxic/anoxic events, surviving weeks to months without oxygen. One of the species known to survive to such extreme condition is the benthic one Ammonia tepida. However the metabolic process by which it succeed in it remains unknown. One hypothesis is that this species would be able to lower its metabolism under oxygen depleted conditions, until the return of better conditions. The aim of the present study is to understand the feeding behaviors of A. tepida under anoxia. For this purpose a laboratory experiment involving incubation with living A. tepida was carried out under controlled oxygen concentrations. The individuals were fed with a pulse of 13C-labeled diatoms (Navicula sp.) and then incubate in oxic or anoxic conditions during 28 days. Along the incubation time, observation of the cell ultrastructure with Transmission Electronic Microscope (TEM) and detection in the cell of the isotopic 13C signal using nanoSIMS, were made. The nanoSIMS (nanoscale Secondary-Ion Mass Spectrometry) is an analytical technique that allows to visualize the incorporation and transfer of isotopically labeled compounds in organisms; thus in our case to follow the ingestion of labeled-diatoms and further transfer of carbon in the cytoplasm of the foraminifera. According to the results acquired in this study, in both conditions the foraminifera directly integrate the diatoms in their cytoplasm during the first hours of the incubation. Then, in oxic conditions, these diatoms are quickly fully degraded, within 3 days, and the 13C-labeled compounds are transferred in the organelles of the cytoplasm. Whereas in anoxia, only a fraction of the diatoms are degraded and the transfer to the foraminifera cytoplasm is weak. These results are confirmed by the δ13C of the foraminifera, measured in bulk by mass spectrometry (GC-MS). In anoxia the δ13C is slightly increasing the first 24h, meaning that the 13C content of the cell increased, and then it remains stable until the end of the experiment. This leads us to assume that the foraminifera stop, or at least strongly lower their metabolic rate under anoxic condition.