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Nicholas Collins
Nicholas Collins

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In physoclist fishes filling of the swimbladder requires acid secretion of gas gland cells to switch on the Root effect and subsequent countercurrent concentration of the initial gas partial pressure increase by back-diffusion of gas molecules in the rete mirabile. It is generally assumed that the rete mirabile functions as a passive exchanger, but a detailed analysis of lactate and water movements in the rete mirabile of the eel revealed that lactate is diffusing back in the rete. In the present study we therefore test the hypothesis that expression of transport proteins in rete capillaries allows for back-diffusion of ions and metabolites, which would support the countercurrent concentrating capacity of the rete mirabile. It is also assumed that in silver eels, the migratory stage of the eel, the expression of transport proteins would be enhanced.

rete 1 pdf free download

Analysis of the transcriptome and of the proteome of rete mirabile tissue of the European eel revealed the expression of a large number of membrane ion and metabolite transport proteins, including monocarboxylate and glucose transport proteins. In addition, ion channel proteins, Ca2+-ATPase, Na+/K+-ATPase and also F1F0-ATP synthase were detected. In contrast to our expectation in silver eels the expression of these transport proteins was not elevated as compared to yellow eels. A remarkable number of enzymes degrading reactive oxygen species (ROS) was detected in rete capillaries.

Our results reveal the expression of a large number of transport proteins in rete capillaries, so that the back diffusion of ions and metabolites, in particular lactate, may significantly enhance the countercurrent concentrating ability of the rete. Metabolic pathways allowing for aerobic generation of ATP supporting secondary active transport mechanisms are established. Rete tissue appears to be equipped with a high ROS defense capacity, preventing damage of the tissue due to the high oxygen partial pressures generated in the countercurrent system.

In physoclist fishes, i.e. in fish in which the embryonic connection of the swimbladder to the esophagus is lost during early development, the swimbladder is filled with gas molecules by diffusion from the blood and from swimbladder gas gland cells [1]. To generate the required high gas partial pressures to drive diffusion gas gland cells in the swimbladder epithelium secrete acid into the blood, switching on the Root effect [2,3,4,5,6]. The resulting initial increase in oxygen partial pressure, the so called single concentrating effect [7], is then in a second step multiplied by countercurrent concentration in the rete mirabile of the swimbladder [6,7,8,9]. The rete has been considered to function by passive diffusion and hydraulic (osmotic) transport [10,11,12], although Steen [13] suggested that lactate may be transported from the venous to the arterial side in the rete mirabile of the European eel. A re-assessment of lactate and water movements in the rete by measurement of hemoglobin and of metabolite concentrations in blood samples collected anterior and posterior to the rete mirabile of the European eel revealed a significant back-diffusion of lactate from venous capillaries to the arterial side, but no significant osmotic gradient and no water movement was detected [14]. This would require presence of lactate transport proteins in the rete, i.e. presence of monocarboxylate carrier proteins [15]. Including the back-diffusion of solutes in the rete and the salting-out effect, i.e. the reduction of gas solubility with increasing solute concentration in blood [16], in model calculations revealed that the back-diffusion of solutes even enhances the countercurrent concentrating capacity of a rete [17]. The possible presence of transport proteins in rete mirabile membranes, indicated by the recorded lactate movements in the rete, therefore could significantly support the countercurrent concentrating ability of the rete and thus enhance the capacity of the rete to generate elevated gas partial pressures. This would imply that the rete mirabile is not just a passive exchanger, and the countercurrent concentrating ability of the rete could not only be modified by changing the surface area of the capillaries, but also by modifying the expression of transport proteins in rete capillaries.

In many fish, the arterial capillaries of the rete mirabile are in intimate contact with the gas gland cells and in close proximity to the venous capillaries of the rete mirabile [18, 19]. Thus, collection of arterial and venous blood samples at the swimbladder side of the rete is difficult without contamination by the secretory activity of gas gland cells. In Anguillidae, such as the European eel, however, the two retia mirabilia of the swimbladder are bipolar and clearly separated from the gas gland cells. Therefore, blood samples can be collected at the arterial entrance and exit of the rete, and at the venous entrance and exit of the rete. For this reason, the eel has become a model species for the analysis of swimbladder physiology [13, 20, 21]. In the eel, each rete consists of about 30,000 to 40,000 arterial capillaries, which on the swimbladder pole of the retia give raise to two or three larger arterial vessels supplying the swimbladder epithelium, consisting of gas gland cells. From there the venous blood returns in two or three larger veins to the retia mirabilia, forming 20,000 to 30,000 venous capillaries, running parallel to the arterial capillaries with a diffusion distance of about 2 μm [22, 23].

The European eel is a catadromous fish spending most of its life cycle as so-called yellow eel in the European freshwater system. In preparation of the spawning migration eels pass the process of silvering to prepare for the transition to seawater. Silver eels then return to the spawning grounds in the Sargasso Sea, a journey taking about 5 to 6 months, perhaps even longer [24]. During silvering, which has been described as a secondary metamorphosis and puberty like event [25, 26], the size of the eel rete mirabile increases, indicating an improvement of the countercurrent concentrating ability [6, 7]. For American eel a two- to three-fold increase in rete length has been reported, and in the Japanese eel a 1.6-fold increase has been detected [27, 28]. Recent tracking studies revealed that migrating silver eels perform daily vertical migrations covering depth changes of several hundred meters [24, 29, 30]. The concomitant changes in hydrostatic pressure significantly affect the volume of the flexible-walled swimbladder, and it has been assumed that swimbladder function is improved during the process of silvering [24, 31]. Previous studies revealed significant changes in the transcriptome and the proteome of swimbladder gas gland cells associated with silvering, although the swimbladder is not involved in any osmoregulatory phenomenon. We therefore hypothesized that the countercurrent concentrating capacity of the rete mirabile, the second essential component of a physoclist swimbladder [1], would also be improved during silvering. We hypothesized that the countercurrent concentrating capacity of the rete mirabile would be supported by the expression of solute transport proteins in rete capillaries. Furthermore, during silvering the expression of these proteins would be enhanced, providing further support for the countercurrent concentration. To test these hypotheses, we analyzed and compared the transcriptome as well as the proteome of rete mirabile tissue of European yellow and silver eels. Our previous studies on gas gland cells could only be performed on separate tissue samples, so that a correlation between transcriptome and proteome could not be tested. We therefore aimed at obtaining both, transcriptome and proteome data from each individual fish, in order to connect transcriptome and proteome data.

On average (5 yellow eels; 6 silver eels), a cDNA library was sequenced at a depth of 16 mio raw reads. Alignment to the European eel reference genome [32] resulted in about 71% mapped gene reads and 32,674 transcripts that could be hit by at least one read in the transcriptome. Comparing the transcriptome of yellow and silver eels, 99 differentially expressed genes were detected at the level of p

Pathway analysis using the Reactome pathway browser revealed that in 25 pathways between 27% and 61% of the in the Reactome database listed genes were transcribed in rete tissue of the European eel (Fig. 1). 59% of cell cycle related genes were transcribed, but also 34% of genes involved in transport of small molecules and 44% of genes connected to vesicle transport. Of note, 43% of the genes involved in signal transduction were transcribed in rete tissue. Of the genes associated with metabolism, 49 out of 140 genes were involved in glucose metabolism and 14 out of 46 genes associated with the pentose phosphate shunt were detected. In addition, 60 out of 233 genes involved in the citric acid cycle and 39 out of 150 genes contributing to the respiratory chain were transcribed in rete tissue. Looking at genes responsible for the formation of the extracellular matrix, 127 out of 330 listed genes were detected in the rete transcriptome.

Percentage of genes of the 25 pathways identified in the Reactome analysis in the transcriptome (blue line) and the proteome (orange line) of European yellow and silver eel rete mirabile tissue. Because only very few genes were differentially expressed between yellow and silver data sets were combined to obtain a clearer picture of genes expressed in rete mirabile tissue. The number gives the total number of genes listed in the Reactome data base for the respective pathway


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