Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis

Department of Genetics, Stanford University School of Medicine, Stanford, CA 94305, USA.
Journal of Experimental Biology (Impact Factor: 3). 10/2012; 215(Pt 19):3467-77. DOI: 10.1242/jeb.070946
Source: PubMed

ABSTRACT Reef-building corals and many other cnidarians are symbiotic with dinoflagellates of the genus Symbiodinium. It has long been known that the endosymbiotic algae transfer much of their photosynthetically fixed carbon to the host and that this can provide much of the host's total energy. However, it has remained unclear which metabolite(s) are directly translocated from the algae into the host tissue. We reexamined this question in the small sea anemone Aiptasia using labeling of intact animals in the light with (13)C-bicarbonate, rapid homogenization and separation of animal and algal fractions, and analysis of metabolite labeling by gas chromatography-mass spectrometry. We found labeled glucose in the animal fraction within 2 min of exposure to (13)C-bicarbonate, whereas no significant labeling of other compounds was observed within the first 10 min. Although considerable previous evidence has suggested that glycerol might be a major translocated metabolite, we saw no significant labeling of glycerol within the first hour, and incubation of intact animals with (13)C-labeled glycerol did not result in a rapid production of (13)C-glucose. In contrast, when Symbiodinium cells freshly isolated from host tissue were exposed to light and (13)C-bicarbonate in the presence of host homogenate, labeled glycerol, but not glucose, was detected in the medium. We also observed early production of labeled glucose, but not glycerol, in three coral species. Taken together, the results suggest that glucose is the major translocated metabolite in dinoflagellate-cnidarian symbiosis and that the release of glycerol from isolated algae may be part of a stress response.

Download full-text


Available from: Ted K. Raab, Jul 03, 2015
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Gorgonian corals are the dominant benthic fauna on many Caribbean reefs, and yet studies on the makeup of the host, or their dinoflagellate symbionts, Symbiodinium spp., are scarce. We investigated the biochemical composition and symbiont parameters in eight gorgonian coral species. Skeletal material, comprised of sclerites and refractory material, was the largest component of gorgonian branches. Relative amounts of sclerites and refractory material varied between species and may explain species level differences in branch flexibility. In gorgonian branches, proteins, present in refractory and cellular material, made up the largest component of organic matter, followed by lipids, while carbohydrates were a minor component. The lipid content in gorgonian organic matter was significantly correlated with Symbiodinium density. In addition, symbiont density in gorgonian branches was probably influenced by the availability of host cells. Knowledge about biochemical parameters of gorgonian corals at ambient environmental conditions will assist in understanding the abundant benthic fauna of many Caribbean coral reefs.
    Journal of Experimental Marine Biology and Ecology 12/2014; 461:275–285. DOI:10.1016/j.jembe.2014.08.016 · 2.48 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Cnidarian–dinoflagellate photosynthetic symbioses are fundamental to biologically diverse and productive coral reef ecosystems. The hallmark of this symbiotic relationship is the ability of dinoflagellate symbionts to supply their cnidarian host with a wide range of nutrients. Many aspects of this association nevertheless remain poorly characterized, including the exact identity of the transferred metabolic compounds, the mechanisms that control their exchange across the host–symbiont interface, and the precise subcellular fate of the translocated materials in cnidarian tissues. This lack of knowledge is mainly attributed to difficulties in investigating such metabolic interactions both in situ, i.e. on intact symbiotic associations, and at high spatial resolution. To address these issues, we illustrate the application of two in situ and high spatial resolution molecular and ion imaging techniques–matrix-assisted laser desorption ionization mass spectrometry imaging (MALDI-MSI) and the nano-scale secondary-ion mass spectrometry (NanoSIMS) ion microprobe. These imaging techniques provide important new opportunities for the detailed investigation of many aspects of cnidarian–dinoflagellate associations, including the dynamics of cellular interactions.
    Zoology 10/2014; 118(2). DOI:10.1016/j.zool.2014.06.006 · 1.60 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Intracellular habitats have been invaded by a remarkable diversity of organisms, and strategies employed to successfully reside in another species' cellular space are varied. Common selective pressures may be experienced in symbioses involving phototrophic symbionts and heterotrophic hosts. Here I refine and elaborate the Arrested Phagosome Hypothesis that proposes a mechanism that phototrophs use to gain access to their host's intracellular habitat. I employ the economic concept of production possibility frontiers (PPF) as a useful heuristic to clearly define the trade-offs that an intracellular phototroph is likely to face as it allocates photosynthetically-derived pools of energy. Fixed carbon can fuel basic metabolism/respiration, it can support mitotic division, or it can be translocated to the host. Excess photosynthate can be stored for future use. Thus, gross photosynthetic productivity can be divided among these four general categories, and natural selection will favor phenotypes that best match the demands presented to the symbiont by the host cellular habitat. The PPF highlights trade-offs that exist between investment in growth (i.e., mitosis) or residency (i.e., translocating material to the host). Insights gained from this perspective might help explain phenomena such as coral bleaching because deficits in photosynthetic production are likely to diminish a symbiont's ability to "afford" the costs of intracellular residency. I highlight deficits in our current understanding of host:symbiont interactions at the molecular, genetic, and cellular level, and I also discuss how semantic differences among scientists working with different symbiont systems may diminish the rate of increase in our understanding of phototrophic-based associations. I argue that adopting interdisciplinary (in this case, inter-symbiont-system) perspectives will lead to advances in our general understanding of the phototrophic symbiont's intracellular niche.
    Frontiers in Microbiology 07/2014; 5:357. DOI:10.3389/fmicb.2014.00357 · 3.94 Impact Factor