Changes in thiamine concentrations, fatty acid composition, and some other lipid-related biochemical indices in Baltic Sea Atlantic salmon (Salmo salar) during the spawning run and pre-spawning fasting

Abstract

Salmonines in the Baltic Sea and North American lakes suffer from thiamine (vitamin B1) deficiency, which is connected to an abundant lipid-rich diet containing substantial amounts of polyunsaturated fatty acids (PUFAs). In the Baltic region, this is known as the M74 syndrome. It affects both adult salmon (Salmo salar) and especially their offspring, impairing recruitment. However, very little is known about the thiamine and lipid metabolism of salmon during feeding and spawning migrations in the Baltic Sea. In this study, salmon females were sampled along the spawning run from the southern Baltic Proper in four locations at sea and finally at spawning in a river at the Bothnian Bay in a year with insignificant M74 mortality. Changes in concentrations of thiamine and its components in muscle, ovaries, and the liver and other biochemical indices potentially relating to lipid and fatty acid metabolism were investigated. The results provide further evidence of the role of peroxidation of PUFAs in eliciting thiamine deficiency in salmon: During the entire spawning run, the muscle total lipid content decreased by 50%, palmitic acid (16:0) by 62%, and docosahexaenoic acid (DHA, 22:6n-3) by 45%. The concentration of total thiamine decreased significantly until the spawning in the liver and ovaries, 66 and 70% respectively. In the muscle, the proportion of thiamine pyrophosphate of total thiamine increased with the use of muscular lipid stores. There was no trend in the concentration of total carotenoids during the spawning run. The doubling of the concentration of hepatic malondialdehyde indicated peroxidation of PUFAs, and the mobilisation of body lipids suppressed the activity of glucose-6-phosphate dehydrogenase, as consumed dietary lipids would also have done.

Model for estimating thiamine deficiency-related mortality of Atlantic salmon (Salmo salar) offspring and variation in the Baltic salmon M74 syndrome

“…How soon, calculated as day-degrees (sum of daily temperature degrees), the first thiamine deficiency symptoms and mortalities are noticeable in yolk-sac fry after hatching is related to the thiamine concentration of the eggs (Amcoff et al 1999;Czesny et al 2009;Keinänen et al 2014). Due to oxidative stress caused by lipid peroxidation and thiamine deficiency (Gibson and Zhang 2002;Vuorinen et al 2020), the concentration of carotenoids, efficient antioxidants (Miki 1991;Shimidzu et al 1996), is also smaller in the eggs of females whose offspring suffer from M74 during the yolk-sac phase (M74 female) than in non-M74 females (Pickova et al 1998(Pickova et al , 2003Lundström et al 1999b). However, carotenoid deficiency does not cause M74 mortality (Koski et al 1999).…”

“…As the lipid content varies by species, being on average higher in sprat than in herring, but also by age and the Baltic Sea areas, dietary lipid content and energy density also vary (Keinänen et al 2012). Docosahexaenoic acid (DHA, 22:6 n-3) is also the prevalent n-3 LC-PUFA in Baltic salmon as in sprat and herring (Keinänen et al 2017(Keinänen et al , 2018Vuorinen et al 2020). However, the fatty acid composition of sprat and herring differs significantly, despite some intra-species differences in them between areas and seasons (Røjbek et al 2014;Keinänen et al 2017).…”

“…The total carotenoid concentration of ovulated unfertilized eggs was measured spectrophotometrically according to Pettersson and Lignell (1999), with slight modifications as described in Vuorinen et al (2020).…”

“…In all, thiamine is principally located in the muscle tissue, the largest tissue in fish. In the muscle of salmon on their spawning run and at spawning, TPP accounted for 80-88% of TotTH (Vuorinen et al 2020). The co-enzyme form TPP in general accounts for the major part of thiamine in vertebrate soft tissues such as the muscle, brain, and liver (Combs and McClung 2017).…”

“…Muscle TPP probably does not easily supply additional thiamine for transportation to developing oocytes because >90% of TPP in the muscle is bound to the enzymes in the mitochondria (Depeint et al 2006). Consequently, the concentration and proportion of THIAM in the muscle of pre-spawning salmon were very low, 0.03-0.13 nmol g −1 and 0.5-1.9%, respectively (Vuorinen et al 2020). During the feeding migration, the smallest THIAM proportions and concentrations of muscle were detected in the fattiest salmon specimens (Keinänen et al unpubl.).…”