Environmental, nutritional and endocrine regulation of metabolic processes in fish
Abstract
Due to seasonal variations in temperature and food availability, fish in temperate regions
should be able to make metabolic adjustments to ensure that enough energy is available
for the maintenance of basal processes. The major aim of this thesis was to elucidate how
the physiology and lipid metabolism of salmonid fish is affected by temperature and food
availability, and to clarify aspects of the endocrine control of lipid metabolism.
In this thesis, the effects of increased temperature or reduced food availability were
studied in salmonids by employing a non-prejudiced metabolomics approach to assess the physiological responses. Detailed information on the abundance of specific amino acids, lipid classes, fatty acids and other metabolites in tissue extracts and plasma was obtained by nuclear magnetic resonance (NMR) based metabolomics. NMR-based metabolomics
were successfully employed and proved to be applicable to studying metabolic fluxes in
fish, providing data on novel and integrated responses. The results show similar changes
in lipid metabolism during food deprivation and elevated temperature. The observed
responses included increased plasma very-low-density lipoprotein (VLDL) and
unsaturated fatty acids (FAs) concurrent with decreased high-density lipoprotein (HDL)
and choline. The changes during starvation also involved changes in amino acids and
glycogen that indicate that amino acids are used for gluconeogenesis in the liver to
preserve glycogen stores.
Growth hormone (GH) has both lipolytic and lipogenic effects. To further elucidate the
mechanisms of GH action on salmonid lipid metabolism, the effects of GH in vivo on the
transcription of several key lipid metabolism enzymes in various tissues were investigated.
GH inhibited the hepatic expression of lipoprotein lipase (LPL) thereby decreasing
hepatic lipid uptake. Hormone-sensitive lipase (HSL) mRNA expression was not
increased by GH in any of the studied tissues, suggesting that the well-known GHinduced
lipolysis is regulated on posttranslational levels in rainbow trout. The regulation
lipid metabolism in salmonids was further investigated by studying direct effects of FAs
and ghrelin on freshly isolated cells from mesenteric adipose tissue and liver. FAs elicited acute negative effects on lipid storage by decreasing lipid uptake via LPL activity in
adipose cells as well as by stimulating lipolysis of stored triglycerides (TG) in liver cells.
Together the results presented in this thesis shows that elevated, suboptimal temperature
and nutritional may have propound effects on important processes as growth, food intake
and the metabolome of salmonid fish, and may lead to a negative energy balance.
Metabolic changes may be mediated by hormonal and nutrient factors acting at gene
expression or enzyme activity level. The results may contribute to better understand lipid deposition patterns in farmed fish and potential effects of climate change on salmonids in the wild and in aquaculture.
Parts of work
Kullgren A, Samuelsson LM, Larsson DGJ, Björnsson BTh, Jönsson Bergman E, 2010. A metabolomics approach to elucidate effects of
food deprivation in juvenile rainbow trout (Oncorhynchus mykiss).
American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 299 (6):R1440-R1448.::doi::10.1152/ajpregu.00281.2010 Kullgren A, Jutfelt F, Fontanillas R, Sundell K, Samuelsson LM, Wiklander K, Kling P, Koppe W, Larsson DGJ, Björnsson BTh, Jönsson E. The impact of temperature on the metabolome and
endocrine metabolic signaling in Atlantic salmon (Salmo salar). Manuscript Kullgren A, Björnsson BTh, Jönsson E. Growth hormone regulates lipid metabolism-related genes in rainbow trout in vivo. Manuscript Kullgren A, Jönsson E. Lipid uptake and mobilization in isolated rainbow trout hepatocytes and adipocytes are affected by fatty acids and temperature. Manuscript
Degree
Doctor of Philosophy
University
University of Gothenburg. Faculty of Science
Institution
Department of Zoology ; Zoologiska institutionen
Disputation
Fredagen den 9 december 2011 kl. 10:00 i Stora föreläsningssalen, Zoologiska Institutionen, Medicinaregatan 18, Göteborg
Date of defence
2011-12-09
Date
2011-11-18Author
Kullgren, Andreas
Keywords
lipids
metabolism
temperature
fasting
growth hormone
ghrelin
NMR
metabolomics
Salmo salar
Oncorhynchus mykiss
Publication type
Doctoral thesis
ISBN
978-91-628-8390-4
Language
eng