Loss of stomach, loss of appetite? Sequencing of the ballan wrasse (Labrus bergylta) genome and intestinal transcriptomic profiling illuminate the evolution of loss of stomach function in fish

Abstract

BackgroundThe ballan wrasse (Labrus bergylta) belongs to a large teleost family containing more than 600 species showing several unique evolutionary traits such as lack of stomach and hermaphroditism. Agastric fish are found throughout the teleost phylogeny, in quite diverse and unrelated lineages, indicating stomach loss has occurred independently multiple times in the course of evolution. By assembling the ballan wrasse genome and transcriptome we aimed to determine the genetic basis for its digestive system function and appetite regulation. Among other, this knowledge will aid the formulation of aquaculture diets that meet the nutritional needs of agastric species.ResultsLong and short read sequencing technologies were combined to generate a ballan wrasse genome of 805 Mbp. Analysis of the genome and transcriptome assemblies confirmed the absence of genes that code for proteins involved in gastric function. The gene coding for the appetite stimulating protein ghrelin was also absent in wrasse. Gene synteny mapping identified several appetite-controlling genes and their paralogs previously undescribed in fish. Transcriptome profiling along the length of the intestine found a declining expression gradient from the anterior to the posterior, and a distinct expression profile in the hind gut.ConclusionsWe showed gene loss has occurred for all known genes related to stomach function in the ballan wrasse, while the remaining functions of the digestive tract appear intact. The results also show appetite control in ballan wrasse has undergone substantial changes. The loss of ghrelin suggests that other genes, such as motilin, may play a ghrelin like role. The wrasse genome offers novel insight in to the evolutionary traits of this large family. As the stomach plays a major role in protein digestion, the lack of genes related to stomach digestion in wrasse suggests it requires formulated diets with higher levels of readily digestible protein than those for gastric species.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4570-8) contains supplementary material, which is available to authorized users.

Expression analyses of digestive enzymes during early development and in adults of the chame fishDormitator latifrons

“…Nevertheless, the expression of pepsin is not present in stomachless species such as ballan wrasse L. bergylta (Hansen et al, ) and is negligible in Atherinops affinis (Logothetis et al, ), due to their lack of a functional stomach. Some studies have shown that stomachless fish such as ballan wrasse (Lie et al, ), zebrafish ( Danio rerio ) and medaka ( Oryzias latipes ) have lost the pepsinogen gene, and this loss is correlated with the lack of a stomach function (acid secretion and pepsin activity) (Castro et al, ). It has been suggested that the source of food and changes in the diet to which these organisms were subjected, acted as a driving force for the loss of the stomach (Castro et al, ).…”

Intestinal Function of the Stomachless Fish, Ballan Wrasse (Labrus bergylta)

“…The dominant expression of Aqp10a and Aqp11 in Segment 1 may be associated with the major digestion and absorption of macronutrients of this section. In some fish species, including the wrasses, triglycerides (TG) are completely hydrolyzed during digestion to free fatty acids and a free glycerol molecule in the intestinal lumen (Lie et al, 2018;Saele et al, 2018). We hypothesize that Aqp10a, which is permeable to glycerol (Madsen et al, 2015), may be involved in glycerol absorption to the enterocytes.…”

“…Furthermore while also lacking pyloric caeca, agastric fish may have a relatively long intestine measuring several times the animal body length (e.g., bighead carp Aristichthys nobilis) (Opuszynski and Shireman, 1991), which increases the overall surface area of the intestine. However, it remains unknown how efficiently nutrients are digested and absorbed in agastric fish with short digestive tracts such as the ballan wrasse (Figure 1) (Deady and Fives, 1995;Figueiredo et al, 2005;Skiftesvik et al, 2014;Lie et al, 2018;Artüz, 2019). It is also unknown if the wider anterior segment of ballan wrasse functions as a food storage area and thus if the intestinal bulb should be considered a pseudogaster.…”

Switching on the light: using metagenomic shotgun sequencing to characterize the intestinal microbiome of Atlantic cod

“…Finally, there have been significant investments to domesticate Atlantic cod for aquaculture purposes. Various factors have prevented this industry to be profitable, for instance through difficulties in immunization of juvenile cod (Samuelsen et al, 2006;Froese and Pauly, 2012), but also through to an inefficient digestion of formulated food of larvae in the prestomach stage (Hamre, 2006;Lie et al, 2018). Providing baseline data of the natural composition of intestinal microbiome in Atlantic cod may help efforts to improve the profitability of this industry.…”