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The rete mirabile: a possible control site for swimbladder function.

ABSTRACT: In a recent study, a large number of transport proteins was detected in the transcriptome and proteome of saline perfused rete mirabile tissue of the European eel. In this study, the data set was reanalyzed for the presence of receptor proteins and proteins involved in intracellular signaling pathways. A large number of expressed receptor proteins and proteins involved in intracellular signal transduction was detected. Several G-protein-coupled receptor signal pathways were significantly enriched in their expression level, in particular receptors and signaling pathways involved in the control of blood flow. The enriched signaling pathways also include pathways involved in trafficking of crucial transport proteins like, monocarboxylate transporters, V-ATPase, and aquaporin. The data, therefore, suggest that the rete mirabile has the capacity to control swimbladder function by regulating blood flow and by modifying countercurrent multiplication.

SUBMITTER: Pelster B

PROVIDER: S-EPMC10209234 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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The rete mirabile: a possible control site for swimbladder function.

Pelster Bernd B

Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology 20230415 3

In a recent study, a large number of transport proteins was detected in the transcriptome and proteome of saline perfused rete mirabile tissue of the European eel. In this study, the data set was reanalyzed for the presence of receptor proteins and proteins involved in intracellular signaling pathways. A large number of expressed receptor proteins and proteins involved in intracellular signal transduction was detected. Several G-protein-coupled receptor signal pathways were significantly enriche ...[more]

PMID: 37060451

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Project description:BackgroundIn 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.ResultsAnalysis 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.ConclusionsOur 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.

Project description:Sébastien Lavoué, Sahat Ratmuangkhwang, Hsuan-Ching Ho, Wei-Jen Chen, and Mohd Nor Siti Azizah (2018) Longfin herrings form a monophyletic, circumtropically distributed family of mostly marine teleost fishes, the Pristigasteridae (Clupeoidei), that includes 38 species classified into nine genera and three main lineages (the Pelloninae, Pristigasterinae, and the genus Ilisha). The external morphology and osteology of the Pristigasteridae provide only a few, sometimes conflicting, informative characters which makes it difficult to reconstruct their phylogeny, but their swimbladder (a visceral gas-filled chamber that has several important functions in the Teleostei) appears to be highly specialized and variable among species. In particular, the swimbladder of most Indo-West Pacific pristigasterid species exhibits one or paired post-coelomic extensions, whereas New World species do not. The presence of these extensions conflicts with the current systematic classification, as they are only found in subsets of different taxa. To examine this conflict, the most comprehensive molecular phylogenetic tree of the Pristigasteridae to date was built using six molecular markers and 21 species. This tree deeply disagreed with the current classification in that it indicated that the subfamilies Pelloninae and Pristigasterinae are not monophyletic and neither are the genera Ilisha, Pellona, and Opisthopterus. Using this tree to infer the evolution of the post-coelomic extensions, it was found that their absence is the ancestral condition in the Pristigasteridae. Indo-West Pacific species with post-coelomic extensions evolved later and form a monophyletic group, inside which species with only one extension form a monophyletic group. The consequences of our findings on the evolution and classification of Pristigasteridae are discussed. We suggest that only species of Pristigasteridae having one or paired post-coelomic extensions should be included in the genus Ilisha.

Project description:Leakiness of the swimbladder wall of teleost fishes must be prevented to avoid diffusional loss of gases out of the swimbladder. Guanine incrustation as well as high concentrations of cholesterol in swimbladder membranes in midwater and deep-sea fish has been connected to a reduced gas permeability of the swimbladder wall. On the contrary, the swimbladder is filled by diffusion of gases, mainly oxygen and CO2 , from the blood and the gas gland cells into the swimbladder lumen. In swimbladder tissue of the zebrafish and the Japanese eel, aquaporin mRNA has been detected, and the aquaporin protein has been considered important for the diffusion of water, which may accidentally be gulped by physostome fish when taking an air breath. In the present study, the expression of two aquaporin 1 genes (Aqp1aa and Aqp1ab) in the swimbladder tissue of the European eel, a functional physoclist fish, was assessed using immunohistochemistry, and the expression of both genes was detected in endothelial cells of swimbladder capillaries as well as in basolateral membranes of gas gland cells. In addition, Aqp1ab was present in apical membranes of swimbladder gas gland cells. The authors also found high concentrations of cholesterol in these membranes, which were several fold higher than in muscle tissue membranes. In yellow eels the cholesterol concentration exceeded the concentration detected in silver eel swimbladder membranes. The authors suggest that aquaporin 1 in swimbladder gas gland cells and endothelial cells facilitates CO2 diffusion into the blood, enhancing the switch-on of the Root effect, which is essential for the secretion of oxygen into the swimbladder. It may also facilitate CO2 diffusion into the swimbladder lumen along the partial gradient established by CO2 production in gas gland cells. Cholesterol has been shown to reduce the gas permeability of membranes and thus could contribute to the gas tightness of swimbladder membranes, which is essential to avoid diffusional loss of gas out of the swimbladder.

Project description:BACKGROUND:Anguillicolidae Yamaguti, 1935 is a family of parasitic nematode infecting fresh-water eels of the genus Anguilla, comprising five species in the genera Anguillicola and Anguillicoloides. Anguillicoloides crassus is of particular importance, as it has recently spread from its endemic range in the Eastern Pacific to Europe and North America, where it poses a significant threat to new, naïve hosts such as the economic important eel species Anguilla anguilla and Anguilla rostrata. The Anguillicolidae are therefore all potentially invasive taxa, but the relationships of the described species remain unclear. Anguillicolidae is part of Spirurina, a diverse clade made up of only animal parasites, but placement of the family within Spirurina is based on limited data. RESULTS:We generated an extensive DNA sequence dataset from three loci (the 5' one-third of the nuclear small subunit ribosomal RNA, the D2-D3 region of the nuclear large subunit ribosomal RNA and the 5' half of the mitochondrial cytochrome c oxidase I gene) for the five species of Anguillicolidae and used this to investigate specific and generic boundaries within the family, and the relationship of Anguillicolidae to other spirurine nematodes. Neither nuclear nor mitochondrial sequences supported monophyly of Anguillicoloides. Genetic diversity within the African species Anguillicoloides papernai was suggestive of cryptic taxa, as was the finding of distinct lineages of Anguillicoloides novaezelandiae in New Zealand and Tasmania. Phylogenetic analysis of the Spirurina grouped the Anguillicolidae together with members of the Gnathostomatidae and Seuratidae. CONCLUSIONS:The Anguillicolidae is part of a complex radiation of parasitic nematodes of vertebrates with wide host diversity (chondrichthyes, teleosts, squamates and mammals), most closely related to other marine vertebrate parasites that also have complex life cycles. Molecular analyses do not support the recent division of Anguillicolidae into two genera. The described species may hide cryptic taxa, identified here by DNA taxonomy, and this DNA barcoding approach may assist in tracking species invasions. The propensity for host switching, and thus the potential for invasive behaviour, is found in A. crassus, A. novaezelandiae and A. papernai, and thus may be common to the group.

Dataset Information

The rete mirabile: a possible control site for swimbladder function.

Publications

The rete mirabile: a possible control site for swimbladder function.

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