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Trimethylamine oxide accumulation in marine animals: relationship to acylglycerol storage

Brad A. Seibel^* and Patrick J. Walsh

NIEHS Marine and Freshwater Biomedical Sciences Center, Rosenstiel School of Marine and Atmospheric Science, Miami, FL 33149, USA

View larger version (14K): [in a new window]   Fig. 1. Diagram showing the possible pathways for trimethylamine (TMA) and trimethylamine oxide (TMAO) production (only abbreviated pathways are drawn). (A) Trimethylalkylammonium compounds (e.g. choline) are degraded to TMA by intestinal microbes (Hebard et al. 1992). (B) Choline is taken up by mitochondria in some animals (Pierce et al., 1997) and converted to glycine betaine via betaine aldehyde. Betaine may subsequently be converted to TMA (Ballantyne, 1997). In both cases (A and B), TMA is oxidized by trimethylamine oxygenase to TMAO.

View larger version (21K): [in a new window]   Fig. 2. (A) Diagram of the glycerolphosphate pathway and phosphatidylcholine synthesis as found in both animals and plants. The bold arrows indicate hypothesized pathways resulting in simultaneous accumulation of acylglycerols and trimethylamine oxide (TMAO) (only abbreviated pathways are drawn). Diacylglycerol (DAG), formed from the derivative glycerol-3-phosphate (DAG), can be shunted towards either acylglycerol (lipid) storage (e.g. triacylglycerol) or phosphatidylcholine (PtdCho) synthesis. The final step in the phosphatidylcholine pathway is reversible. The back reaction may occur to a significant extent so that diacylglycerol is formed from phosphatidylcholine and subsequently stored for seasonal or reproductive energy reserves (see Gur and Harwood, 1991). Choline, thus released, is oxidized to TMAO and either stored or excreted. (B) In some plants, PtdCho is produced by methylation of ethanolamine and may subsequently be hydrolysed for release of DAG and choline. DAG in plants is important during growth for the formation of photosynthetic membrane glycolipids. Choline, thus released, is oxidized to glycine betaine (Hitz et al. 1981). (C) In chenopods (e.g. spinach and sugarbeet), choline is synthesized directly from ethanolamine and, thus, appears to be a specific adaptation for glycine betaine accumulation during drought and salt-stress (Weretilnyke et al., 1995). The enzymes involved in the pathways illustrated are numbered: (1) glycerol-3-phosphate (G3P) is converted to phosphatidic acid by the successive actions of G3P acyltransferase and 1-acylglycerol-3-phosphate acyltransferase; (2) phosphatidic acid phosphatase; (3) 1,2-diacylglycerol:choline phosphotransferase; (4) diacylglycerol acyltransferase; (5,6) carnitine palmitoyl transferases I and II; (7) trimethylamine oxygenase; (8) choline monoxygenase; (9) betaine aldehyde dehydrogenase; (10) P-choline phosphatase. TMA, trimethylamine; P-choline, phosphocholine.

View larger version (13K): [in a new window]   Fig. 3. Trimethylamine oxide content (y, mmol kg–1; see Fig. 4) in mantle muscle tissue is significantly correlated with digestive gland lipid content (x) in cephalopods (y=2.90x1.18, r=0.59, P<0.05). We were unable to analyze trimethylamine oxide (TMAO) content as a function of total lipid content because of the variable presentation of lipid data in the literature. Lipid data were taken from Blanchier and Boucaud-Camou (1984), Hayashi (1989, 1996), Hayashi and Kawasaki (1985), Kristensen (1984), Phillips et al. (2001), Piatkowski and Hagen (1994), Pollero and Iribarne (1988) and Semmens (1998). In many cases, lipid and TMAO data were taken from different species, and possibly different maturity stages, of the same genus. (1) Octopus; (2) Loligo; (3) Galiteuthis; (4) Sepia; (5) Illex; (6) Berryteuthis; (7) Moroteuthis; (8) Gonatopsis; (9) Todarodes; (10) Gonatus. There are conflicting reports regarding the digestive gland lipid content of Thysanoteuthis, a squid that also contains high TMAO concentrations (Hayashi, 1996; Yuneva et al., 1994). Many of the genera plotted here are closely related to each other (see Fig. 4). Therefore, phylogenetic independence of the data should not be assumed.

View larger version (25K): [in a new window]   Fig. 4. Mantle muscle trimethylamine oxide (TMAO, mmol kg–1) measured according to Wekell and Barnett (1991), minimum depth of occurrence (MDO, m) and capture depth (CD, m) of cephalopods listed according to their phylogenetic associations (see Carlini and Graves, 1999). Values are corrected for the dilution of tissue with extracellular ammonium concentrations in some species (see text). Nodes are numbered for reference in the text. Numbers in parentheses are from Hebard et al. (1982) or Kelly and Yancey (1999).

View larger version (21K): [in a new window]   Fig. 5. Mantle muscle trimethylamine oxide (TMAO) content (mmol kg–1; squares) increases (b=0.33) in proportion to digestive gland mass (% body mass; circles; b=0.25) and lipid mass (% body mass; plus signs; b=0.47) through ontogeny (size; g) in gonatid squid (Cephalopoda). The data for TMAO content are from Kelly and Yancey (1999) and B. A. Seibel (unpublished results). Body masses for the TMAO scaling analysis (squares) for Gonatopsis borealis and Berryteuthis magister were estimated at the mean adult body mass for each species (Hayashi, 1989; Hayashi and Yamamoto, 1987). Digestive gland and lipid masses were taken from various sources: Gonatus onyx (B. A. Seibel, personal observation), Gonatus fabricii (Arkhipkin and Bjorke, 1999), Gonatopsis borealis (Hayashi, 1989) and Berryteuthis magister (Hayashi and Yamamoto, 1987). All species appear to fall on the same scaling line despite differences in maximum body sizes. The apparent correlation between lipid content (or digestive gland mass) and TMAO content in gonatid squid is hypothesized to result from the requirement for phosphatidyl choline hydrolysis to produce diacylglycerol for lipid storage. The choline thus released is oxidized to TMAO.