Article

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: 2.9). 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.

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    • "Genes related to the catabolism of sugar alcohols, such as glycerol and inositol, were also observed in the bacteria genome. Both glycerol and inositol are important photosynthetic products that are released by symbiotic Symbiodinium algae and are used by corals [29]. The presence of genes related to the use of these compounds as energy sources demonstrates the adaptation of Kocuria sp. "
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    • "Genes related to the catabolism of sugar alcohols, such as glycerol and inositol, were also observed in the bacteria genome. Both glycerol and inositol are important photosynthetic products that are released by symbiotic Symbiodinium algae and are used by corals [29]. The presence of genes related to the use of these compounds as energy sources demonstrates the adaptation of Kocuria sp. "
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    • "The photosynthetic dinoflagellate endosymbionts, genus Symbiodinium, reside in specialized vacuoles (symbiosomes) within host coral cells (Fig. 1a). They produce photosynthetic products, including glucose and amino acids (Whitehead and Douglas, 2003; Burriesci et al., 2012), which are translocated across the symbiosome to the host and can support more than 100% of the host's metabolic requirements (Davy et al., Received 13 November, 2015; revised 17 December, 2015; accepted 22 December, 2015 Cellular Microbiology (2016) doi:10.1111/cmi.12564 and transcriptomic resources are rapidly becoming available for corals, Aiptasia and Symbiodinium (Sunagawa et al., 2009; Shinzato et al., 2011; Bayer et al., 2012; Lehnert et al., 2012; Baumgarten et al., 2013; Shoguchi et al., 2013; Lehnert et al., 2014; Baumgarten et al., 2015; Lin et al., 2015), increasing the power of the other " omics " approaches, such as metabolomics and proteomics, to investigate the physiology of the cnidarian –dinoflagellate symbiosis (Meyer and Weis, 2012). "
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