Hormonal control of tryptic enzyme activity in Atlantic cod larvae (Gadus morhua): Involvement of cholecystokinin during ontogeny and diurnal rhythm

Abstract

Please cite this article as: Tillner, Robert, Rønnestad, Ivar, Harboe, Torstein, Ueberschär, Bernd, Hormonal control of tryptic enzyme activity in Atlantic cod larvae (Gadus morhua): Involvement of cholecystokinin during ontogeny and diurnal rhythm, Aquaculture (2013Aquaculture ( ), doi: 10.1016Aquaculture ( /j.aquaculture.2013 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT AbstractThe ontogenetic development of the gut hormone cholecystokinin (CCK) and the key proteolytic enzyme trypsin was described in Atlantic cod larvae (Gadus morhua) from first-feeding until 38 days post first-feeding (dpff). CCK is known to play a major role in the endocrine control of digestive processes in mammals and adult fish, but its regulatory role in the larval stages of marine fish is largely unknown. Only small amounts of CCK were found in the body (excluding head) in cod larvae at first-feeding, but CCK levels increased exponentially with development, suggesting a more pronounced role of CCK during ontogeny. Tryptic enzyme activity increased slightly until a standard length of ca. 8 mm (approx. 33 days dpff) with a significant increase in larvae larger than 8 mm standard length, indicating limited digestive capacity in the early stages. To entangle the short-term feedback mechanism between CCK and tryptic enzyme activity, we conducted a 12 hour feeding experiment at 21 dpff. Cod larvae receiving only algae revealed a noticeable response in tryptic enzyme activity within two hours in the morning, whereas larvae fed algae and rotifers at the same time showed a slightly delayed response up to four hours. Tryptic enzyme activity remained low in the group receiving only algae as well as the two fed groups in the afternoon. No reaction in tryptic enzyme activity was observed in larvae that received a second meal of rotifers in the afternoon, indicating limited regulatory and digestive capacity to handle several meals in a short period. CCK levels remained relatively constant throughout the day but increased in the afternoon in all three groups when tryptic enzyme activity was low, suggesting that a negative feedback mechanism between CCK and tryptic enzyme activity is present in larval cod at least from 21 dpff.

The Neuroendocrine Regulation of Food Intake in Fish: A Review of Current Knowledge

“…The first direct evidence of the actions of CCK on feeding was provided by injections in goldfish (Himick and Peter, 1994), followed by cloning of goldfish CCK cDNA (Peyon et al, 1998) and the demonstration of periprandial variations in CCK mRNA expression levels (Peyon et al, 1999). Subsequently, a number of studies have characterized CCK in several fish, including other Cypriniformes (e.g., common carp Zhong et al, 2013; zebrafish Koven and Schulte, 2012; Tian et al, 2015; grass carp; blunt snout bream Ping et al, 2013; Ji et al, 2015), Characiformes (e.g., cavefish Wall and Volkoff, 2013, dourado Pereira et al, 2015; Volkoff et al, 2016, thin dogfish Oligosarcus hepsetus Vieira-Lopes et al, 2013, pirapitinga Volkoff, 2015a, red-bellied piranha Volkoff, 2014a, pacu Volkoff et al, 2017), Salmoniformes (e.g., Atlantic salmon Valen et al, 2011), Gadiformes (Atlantic cod Tillner et al, 2013), Perciformes [e.g., yellowtail (Furutani et al, 2013; Hosomi et al, 2014); Astatotilapia burtoni (Grone et al, 2012); cunner (Babichuk and Volkoff, 2013; Hayes and Volkoff, 2014); sea bass (Tillner et al, 2014); yellow croaker ( Larimichthys crocea ) (Cai et al, 2015); white sea bream, Diplodus sargus (Micale et al, 2012, 2014)], Pleuronectiformes (e.g., winter flounder (MacDonald and Volkoff, 2009a), Atlantic halibut Kamisaka et al, 2001, olive flounder Kurokawa et al, 2000) and Siluriformes (channel catfish Peterson et al, 2012). …”

Effects of dietary protein levels on activities of protease and expression of ingestion and protein digestion‐related genes in Nile tilapia juveniles

“…It has been suggested that ingested protein may have a regulatory function by competing as a substrate for trypsin, thereby preventing the inactivation of the cck‐releasing factor (Liddle, 2000; Rønnestad, Kamisaka, Conceição, Morais, & Tonheim, 2007). In this sense, studies in Gadus morhua larvae have suggested that a negative feedback mechanism is present between cck and trypsin activity (Tillner, Rønnestad, Harboe, & Ueberschär, 2013).…”

Digestive enzymatic activity during ontogenetic development in zebrafish (Danio rerio)

“…Quantitative assessment of digestive enzymes, paralleled to histo‐morphological development of digestive system, could represent a first step towards the study of hormonal mechanisms (i.e., by cholecystokinin, Micale et al, ; Tillner et al, ) involved in digestive processes during ontogeny in zebrafish. Moreover, during the larval period all organs and systems are functional, making larvae physiologically equivalent to adults.…”