Structural and Functional Components of the Skate Sensory Organ Ampullae of Lorenzini

Abstract

The skate, a cartilaginous fish related to sharks and rays, possesses a unique electrosensitive sensory organ known as the ampullae of Lorenzini (AoL). This organ is responsible for the detection of weak electric field changes caused by the muscle contractions of their prey. While keratan sulfate (KS) is believed to be a component of a jelly that fills this sensory organ and has been credited with its high proton conductivity, modern analytical methods have not been applied to its characterization. Surprisingly, total glycosaminoglycan (GAG) analysis demonstrates that the KS from skate jelly is extraordinarily pure, containing no other GAGs. This KS had a molecular weight of 20 to 30 kDa, consisting primarily of N-linked KS comprised mostly of a monosulfated disaccharide repeating unit, →3) Gal (1→4) GlcNAc6S (1→. Proteomic analysis of AoL jelly suggests that transferrin, keratin, and mucin serve as KS core proteins. Actin and tropomyosin are responsible for assembling the macrostructure of the jelly, and parvalbumin α-like protein and calreticulin regulate calcium and potassium channels involved in the transduction of the electrical signal, once conducted down the AoL by the jelly, serving as the molecular basis for electroreception.

Electro‐Stimulation, a Promising Therapeutic Treatment Modality for Tissue Repair: Emerging Roles of Sulfated Glycosaminoglycans as Electro‐Regulatory Mediators of Intrinsic Repair Processes

“…[ 55 ] In nature, protons (H(+)) can mediate metabolic processes through enzymatic reactions. A KS substituted PG‐mucin‐like glycoconjugate gel isolated from the Ampullae of Lorenzini, a sensory pore‐like system present on the surface of the skin of elasmobranch fish species (sharks, rays, skates), is the best proton detection polymer known in Nature [ 56 ] ( Figure ). KS in such mucinous deposits equips coupled neurosensory networks in the fish skin with the ability to detect electric fields generated by the muscular activity of preyfish species, a process known as electro‐location [ 47 ] and is used to hunt prey fish under turbid water conditions of poor visibility.…”

“…KS‐PGs are the most sensitive proton detection molecules known in nature facilitating the process of electro‐location in the elasmobranch sharks, skates, and rays (Figure 8) and in two terrestrial animals, the duck billed platypus ( Figure ) and long and short nosed echidna of Australia ( Figure ), as well as electro‐communication in a number of fish species. [ 55,56,65 ] The predominance of KS substituted molecules in neural tissues also testifies to the unique functional properties conveyed by this GAG in sensory processes. [ 25,46,47,55,56 ] In weakly electric fish species which employ electro‐location or electro‐communication, a characteristic electric oscillatory discharge is generated and emitted by a pacemaker organ.…”

“…[ 55,56,65 ] The predominance of KS substituted molecules in neural tissues also testifies to the unique functional properties conveyed by this GAG in sensory processes. [ 25,46,47,55,56 ] In weakly electric fish species which employ electro‐location or electro‐communication, a characteristic electric oscillatory discharge is generated and emitted by a pacemaker organ. This electrical discharge can be modulated in terms of its amplitude, frequency and the waveform of the signal elicited and other fish can interpret this signal which thereby forms a sophisticated means of social communication.…”

Structural Characteristics and Proton Conductivity of the Gel Within the Electrosensory Organs of Cartilaginous Fishes

“…AoL gel extracted from three fish species demonstrated extremely high proton conductivity, higher than that of any other reported biological material (8). It has been proposed that keratan sulfate, a glycosaminoglycan, is a component of AoL gel and responsible for conferring the substance's proton conductive properties (8,9). Various studies have attempted to uncover the complete molecular makeup of AoL gel, most with a focus on polysaccharides and proteins (9)(10)(11).…”

“…It has been proposed that keratan sulfate, a glycosaminoglycan, is a component of AoL gel and responsible for conferring the substance's proton conductive properties (8,9). Various studies have attempted to uncover the complete molecular makeup of AoL gel, most with a focus on polysaccharides and proteins (9)(10)(11). Cellular contamination during AoL gel extraction, however, makes the interpretation of proteomic datasets challenging.…”