A Holistic View of Dietary Carbohydrate Utilization in Lobster: Digestion, Postprandial Nutrient Flux, and Metabolism

Abstract

Crustaceans exhibit a remarkable variation in their feeding habits and food type, but most knowledge on carbohydrate digestion and utilization in this group has come from research on few species. The aim of this study was to make an integrative analysis of dietary carbohydrate utilization in the spiny lobster Panulirus argus. We used complementary methodologies such as different assessments of digestibility, activity measurements of digestive and metabolic enzymes, and post-feeding flux of nutrients and metabolites. Several carbohydrates were well digested by the lobster, but maize starch was less digestible than all other starches studied, and its inclusion in diet affected protein digestibility. Most intense hydrolysis of carbohydrates in the gastric chamber of lobster occurred between 2–6 h after ingestion and afterwards free glucose increased in hemolymph. The inclusion of wheat in diet produced a slow clearance of glucose from the gastric fluid and a gradual increase in hemolymph glucose. More intense hydrolysis of protein in the gastric chamber occurred 6–12 h after ingestion and then amino acids tended to increase in hemolymph. Triglyceride concentration in hemolymph rose earlier in wheat-fed lobsters than in lobsters fed other carbohydrates, but it decreased the most 24 h later. Analyses of metabolite levels and activities of different metabolic enzymes revealed that intermolt lobsters had a low capacity to store and use glycogen, although it was slightly higher in wheat-fed lobsters. Lobsters fed maize and rice diets increased amino acid catabolism, while wheat-fed lobsters exhibited higher utilization of fatty acids. Multivariate analysis confirmed that the type of carbohydrate ingested had a profound effect on overall metabolism. Although we found no evidence of a protein-sparing effect of dietary carbohydrate, differences in the kinetics of their digestion and absorption impacted lobster metabolism determining the fate of other nutrients.

Molecular, Biochemical, and Dietary Regulation Features of α-Amylase in a Carnivorous Crustacean, the Spiny Lobster Panulirus argus

“…It should be noted that one assumption of our approach is that phenotypic or activity differences in other activities involved (i.e., other starch degrading enzymes) among individual are similar or equally distributed among the experimental groups. Nutritional studies in different spiny lobsters have provided evidence that a gradual digestion of carbohydrates and liberation of glucose to the hemolymph positively impacts their post-absorptive utilization [ 21 , 22 ]. Thus, amylase polymorphism in lobster may be influenced by selective forces toward less carbohydrate digestion.…”

“…The release of free glucose into the gastric juice of lobsters occurs soon after ingestion [ 22 ], and may play a role in α-amylase regulation. While in some insects free glucose suppress α-amylase activity, no glucose repression (or starch induction) has been observed in others [ 82 ], indicating that this is a species-specific phenomenon.…”

“…A continuous flow of buffer is maintained through the external chamber by a high precision peristaltic pump (Ismatec, Idex Corp.), which allows the constant removal of digestion products while the internal chamber is continually agitated by a magnetic stirrer. Two carbohydrates were selected as substrates (wheat and maize flour) as significant differences in digestibility were found between them in a previous study [ 22 ]. Five digestions per phenotype per carbohydrates source (30 digestions) were performed.…”

“…However, in other studies the α-amylase activity of some carnivorous crustaceans [ 19 , 20 ] including spiny lobsters [ 8 , 11 , 18 ] has been observed as high as in herbivorous or omnivorous crustaceans. This high α-amylase activity in spiny lobsters seems also to contradict the limited metabolic use of dietary carbohydrates (e.g., high and prolonged hyperglycemia after feeding) [ 21 , 22 ], probably because reduced activity of enzymes involved in both glycolysis and glycogen synthesis [ 22 ].…”

Carbohydrates digestion and metabolism in the spiny lobster (Panulirus argus): biochemical indication for limited carbohydrate utilization

“…However, there is no evidence of a significant use of CHs for energy in spiny lobsters, though some energy appears to be derived from glycogen of the digestive gland (DG) during short term fasting ( Simon & Jeffs, 2013 ). P. argus is currently supposed to use preferentially proteins and lipids in energy metabolism ( Perera et al, 2005 ), and studies in this and other spiny lobster species have provided indication that several CHs are well digested but poorly utilized ( Simon, 2009a ; Simon, 2009b ; Simon, 2009c ; Simon & Jeffs, 2013 ; Rodríguez-Viera et al, 2014 ). The metabolism of other crustaceans such as penaeid shrimps is also directed to the use of proteins and lipids for energy, but CHs can spare dietary proteins to a certain extent ( Cuzon et al, 2000 ).…”