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First published online November 17, 2005
Journal of Experimental Biology 208, 4355-4361 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01877

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Cross-kingdom hormonal signaling: an insight from thyroid hormone functions in marine larvae

Andreas Heyland^* and Leonid L. Moroz

The Whitney Laboratory for Marine Bioscience and Department of Neuroscience, University of Florida, FL, 32080 USA

View larger version (36K): [in a new window]   Fig. 1. (A) A hypothesis for iodine-based cross-kingdom communication in marine ecosystems. Marine organisms incorporate iodine into an organic matrix (organification) and synthesize thyroid hormone (TH)-related signaling molecules, which are then shuttled through the food chain (phytoplankton to zooplankton). This hypothesis is supported by previously published evidence and our own new data (see Fig. 2) of TH-like molecules being present in marine algae and various marine invertebrates and their larval forms. (B) One functional aspect of this cross-kingdom communication is the involvement of TH-related compounds in development to metamorphosis of various marine invertebrate larvae, represented schematically in B for molluscs (veliger larvae) and echinoderms (pluteus larvae). New evidence suggests that THs are used as developmental signals by larvae and that the primary source may be exogenous (Chino et al., 1994; Heyland and Hodin, 2004), although we were able to find evidence for endogenous synthesis as well (Heyland and Hodin, 2004). The role of THs in metamorphosis per se remains to be elucidated. The blue frame indicates larval development (L) and the red frame metamorphic development with metamorphic competence (C) and settlement (S). Please note that here we are using the term THs generically for thyroid-like hormones, since the specific chemical identification of THs in these lineages requires further confirmation using microanalytical methods (e.g. mass spectrometry and NMR). Images of echinoid larvae modified from Hyman (1995).

View larger version (10K): [in a new window]   Fig. 2. Various algae species commonly used as larval nutrition in laboratory cultures contain thyroxine. We reared replicate samples of algae of three species [Dunaliella tertiolecta (D. tert.), Isochrysis aff. galbana (T-ISO) and Rhodomonas lens (R. lens)] at the coastal research center (WHOI) in Woods Hole (MA, USA) in summer 2002 in 25 l containers using protocols previously described by McEdward and Herrera (1999), although adapted for large-scale use. Sterile starters for all three algae species were obtained from Dr A. D. Anderson's laboratory (Woods Hole Oceanographic Institute, MA, USA). After collection of replicate samples we performed methanol:chloroform extractions and separated small molecular species using Amicon® (Bedford, MA, USA) Ultra-15 Centrifugal Filter Device (5 kDa) and then dried samples down in a Speed-VacTM. We re-dissolved pellets in 50 µl 0.01 mol l–1 NaOH and measured thyroxine using ELISA (Total Thyroxine (Total T4) ELISA Kit Alpha Diagnostics, San Antonio, TX, USA) following the manufacturer's instructions. We determined total protein content for samples using the Micro BCATM Protein Assay Kit from Pierce (Rockford, IL, USA). Although T-ISO has an approximately 10 times smaller cell volume than D. tert. it contains approximately the same amount of thyroxine [T4 standardized by protein content (mg dl–1 g–1 protein)]. Differences in TH content of these algae may reflect differential effects of these algae on larval development and morphogenesis. Values are means ± 1 S.E.M. (N=3). Asterisks indicate significant difference in hormone content between samples using Student's t-test, P<0.05.