For an evaluation of effects of seasonal cold acclimation and evolutionary cold adaptation on protein synthesis

It is commonly accepted that polar marine invertebrates and fish have slow annual growth rates compared to animals from lower latitudes. The first intuitively appealing explanation is that temperature slows down physiological rates in the cold, but this explanation ignores the possibility that over the course of evolution, polar species may have achieved some degree of compensation for the rate-limiting effects of low temperature (Clarke and North, 1991). Recent evidence demonstrates, in fact, that cold-adapted invertebrates and fish of the Southern Ocean reach growth rates during the short Antarctic summer similar to those of their counterparts from temperate regions (Brey and Clarke, 1993; Arntz et al., 1994; Kock and Everson, 1998; Peck, 2002). More recently, interest has focused on protein synthesis in polar species because growth and cellular functioning in tissues are closely related to protein turnover. These studies provided evidence that whole body protein synthesis rates in vivo (Whiteley et al., 1996; Robertson et al., 2001; Marsh et al., 2001; Fraser et al., 2002) are similar to those observed in temperate species. Enabling of the protein synthesis machinery to function at very low ‘operating temperatures’ in vivo has been suggested to be brought about by elevated tissue RNA:protein ratios (milligrams RNA per gram protein). Accordingly, this parameter is commonly used as an indirect measure of the in vivo protein synthesis capacity of a tissue (Waterlow et al., 1978; Sugden and Fuller, 1991; Houlihan, 1991). Increased RNA:protein ratios have been found upon cold acclimation or during winter in various tissues of fish, and for the last two decades this finding has been interpreted to reflect cold compensation of RNA translational activities (kRNA in vivo, defined as grams protein synthesized in vivo per gram RNA per day, also known as RNA translational efficiency), at low temperatures (Goolish et al., 1984; Foster et al., 1992; Foster et al., 1993; Mathers et al., 1993; McCarthy and Houlihan, 1997; McCarthy et al., 1999). Accordingly, it seems very tempting to extrapolate this interpretation to cold-adapted stenotherms from polar regions. The increase in RNA:protein ratios in Antarctic species reflected by increased RNA levels in cold stenotherms from the Southern Ocean (Whiteley et al., 2001; Robertson et al., 2001; Marsh et al., 2001; Fraser et al., 2002) has in fact been suggested to counteract a thermally induced reduction in RNA translational efficiency in vivo. These interpretations imply that in vivo translational efficiency falls in the cold because of a reduction in individual biochemical processes involved in protein synthesis. Such a decrement has never been demonstrated. Synthesis and maintenance of higher RNA levels to counteract the negative effect of cold temperatures on translational activity may further imply higher costs of protein synthesis in the cold. Fraser et al. (2002) proposed that maintaining considerably elevated tissue The Journal of Experimental Biology 208, 2409-2420 Published by The Company of Biologists 2005 doi:10.1242/jeb.01632