Acidic Digestion in a Teleost: Postprandial and Circadian Pattern of Gastric pH, Pepsin Activity, and Pepsinogen and Proton Pump mRNAs Expression

Abstract

Two different modes for regulation of stomach acid secretion have been described in vertebrates. Some species exhibit a continuous acid secretion maintaining a low gastric pH during fasting. Others, as some teleosts, maintain a neutral gastric pH during fasting while the hydrochloric acid is released only after the ingestion of a meal. Those different patterns seem to be closely related to specific feeding habits. However, our recent observations suggest that this acidification pattern could be modified by changes in daily feeding frequency and time schedule. The aim of this study was to advance in understanding the regulation mechanisms of stomach digestion and pattern of acid secretion in teleost fish. We have examined the postprandial pattern of gastric pH, pepsin activity, and mRNA expression for pepsinogen and proton pump in white seabream juveniles maintained under a light/dark 12/12 hours cycle and receiving only one morning meal. The pepsin activity was analyzed according to the standard protocol buffering at pH 2 and using the actual pH measured in the stomach. The results show how the enzyme precursor is permanently available while the hydrochloric acid, which activates the zymogen fraction, is secreted just after the ingestion of food. Results also reveal that analytical protocol at pH 2 notably overestimates true pepsin activity in fish stomach. The expression of the mRNA encoding pepsinogen and proton pump exhibited almost parallel patterns, with notable increases during the darkness period and sharp decreases just before the morning meal. These results indicate that white seabream uses the resting hours for recovering the mRNA stock that will be quickly used during the feeding process. Our data clearly shows that both daily illumination pattern and feeding time are involved at different level in the regulation of the secretion of digestive juices.

Integrative Physiology of Fasting

“…23C and 23D) (40,185,367,379,486,600). Burmese pythons cease acid production even before the last remnants of the meal (mats of hair) have exited the stomach (499).…”

“…Feeding triggers the rapid increase in HCl production that acidifies the gastric lumen within 6 h (40,600). Given that the proteolytic enzyme pepsin requires an acidic lumen to be activated (from pepsinogen), pepsin activity is similarly regulated with fasting and feeding (118,600). Considering the high cost of HCl production (stoichiometry of one ATP hydrolyzed per H + pumped), the selective advantage of this mode of HCl regulation is the reduction in daily energy expenditure during long predicted episodes of fasting (409, 445, 486).…”

“…In contrast, the white sea bream and python maintain a near neutral gastric pH while fasting, experience a rapid drop in pH during digestion, and then curtail acid production with the emptying of the stomach. Figures are drawn, with permission, from data presented in (424,486,599,600).…”

Neuroendocrine control of appetite in Atlantic halibut (Hippoglossus hippoglossus): Changes during metamorphosis and effects of feeding

“…For altricial-gastric species, a crucial change during development is the remodelling of the GI tract during metamorphosis and the appearance of a functional stomach, capable of an adult mode of monogastric digestion (Darias et al, 2007;Douglas et al, 1999;Gomes et al, 2014;Murray et al, 2006;Yúfera et al, 2012). During larval stages, the GI tract has a lower processing capacity, including lower digestibility for proteins (Rønnestad et al, 2007) and probably less developed systems controlling gut transit time and ingestion rate (Rønnestad et al, 2013).…”

Circadian cycle of digestive enzyme production at fasting and feeding conditions in Nile tilapia, Oreochromis niloticus (Actinopterygii: Perciformes: Cichlidae)

“…The photoperiod is the most important factor that entrains animal rhythms, including enzymatic secretion cycles, tied to the daily melatonin rhythms (Bromage et al 2001). Fish exhibit photoperiod-dependent circadian cycles of several processes, including locomotion (zebrafi sh; Zhdanova et al 2001), development (zebrafi sh; Danilova et al 2004), growth (rainbow trout; Falcón et al 2003), reproduction (salmon; Amano et al 2000Amano et al , 2004Senegal sole;Vera et al 2007), control and regulation of reproductive hormones and melatonin (European seabass; Bayarri et al 2004), and digestive enzyme activity (Yúfera et al 2012). Also, they have oscillators and circadian photo transduction drag mechanisms, suggesting that circadian pacemaker functions can be spread throughout the animal (zebrafi sh; Cahill 2002).…”