Abstract
Using Illumina sequencing, transcriptional changes occurring during silvering in swimbladder tissue of the European eel have been analyzed by comparison of yellow and silver eel tissue samples. Functional annotation analysis based on GO terms revealed significant expression changes in a number of genes related to the extracellular matrix, important for the control of gas permeability of the swimbladder, and to reactive oxygen species (ROS) defense, important to cope with ROS generated under hyperbaric oxygen partial pressures. Focusing on swimbladder tissue metabolism, levels of several mRNA species encoding glucose transport proteins were several-fold higher in silver eels, while enzymes of the glycolytic pathway were not affected. The significantly higher steady state level of a transcript encoding for membrane bound carbonic anhydrase, however, suggested that CO2 production in the pentose phosphate shunt and diffusion of CO2 was of particular importance in silver eel swimbladder. In addition, the mRNA level of a large number of genes related to immune response and to sexual maturation was significantly modified in the silver eel swimbladder. The modification of several processes related to protein metabolism and transport, cell cycle, and apoptosis suggested that these changes in swimbladder metabolism and permeability were achieved by increasing cell turn-over. The impact of an infection of the swimbladder with the nematode Anguillicola crassus has been assessed by comparing these expression changes with expression changes observed between uninfected yellow eel swimbladder tissue and infected silver eel swimbladder tissue. In contrast to uninfected silver eel swimbladder tissue, in infected tissue the mRNA level of several glycolytic enzymes was significantly elevated, and with respect to extracellular matrix, several mucin genes were many-fold higher in their mRNA level. Modification of many immune related genes and of the functional categories “response to DNA damage stimulus” and “cellular response to stress” illustrated the damaging effect of the nematode infection. This study has identified a range of cellular processes in the swimbladder of silver eels that appear to be altered by nematode infection. These altered cellular processes could contribute to detrimental changes in swimbladder function that, in turn, may lead to impairment of spawning migration.
Highlights
The European eel Anguilla anguilla is a catadromous fish spending most of its lifetime as yellow eel in the European freshwater system, and returning to the Sargasso Sea for reproduction
We focused on transcriptional changes of genes related to (1) glucose metabolism and (2) ion exchange, which are required for acid production and release in order to switch on the Root effect for gas secretion (Pelster and Randall, 1998; Pelster, 2013); (3) angiogenesis, required for appropriate blood supply to the swimbladder (Kleckner, 1980a); (4) reactive oxygen species (ROS) defense, required to avoid oxidative stress related to hyperbaric oxygen tensions (Morris and Albright, 1981, 1984; Pelster, 2001; Lushchak and Semchyshyn, 2012); (5) extracellular matrix, involved in reducing diffusional gas loss from the swimbladder (Kleckner, 1980a,b; Yamada et al, 2001); (6) immune response, required to defeat the nematode infection (Lefebvre et al, 2011, 2013); and (7) maturation, which occurs in silver eels during spawning migration (Dufour et al, 2003)
Silvering is connected to large scale transcriptional changes in swimbladder tissue, and 78% of the affected genes were elevated in their transcriptional level
Summary
The European eel Anguilla anguilla is a catadromous fish spending most of its lifetime as yellow eel in the European freshwater system, and returning to the Sargasso Sea for reproduction. The increase in oxygen and CO2 partial pressures required to drive the diffusion of these gas molecules into the swimbladder is achieved by acidification of the blood via lactic acid and CO2 release from swimbladder gas gland cells, which reduces the oxygen carrying capacity of the hemoglobin. This so-called single concentrating effect is subsequently multiplied by countercurrent multiplication in the rete mirabile (Pelster and Randall, 1998; Pelster, 2009, 2013)
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