Proton conductivity in ampullae of Lorenzini jelly

Abstract

In 1678, Stefano Lorenzini first described a network of organs of unknown function in the torpedo ray-the ampullae of Lorenzini (AoL). An individual ampulla consists of a pore on the skin that is open to the environment, a canal containing a jelly and leading to an alveolus with a series of electrosensing cells. The role of the AoL remained a mystery for almost 300 years until research demonstrated that skates, sharks, and rays detect very weak electric fields produced by a potential prey. The AoL jelly likely contributes to this electrosensing function, yet the exact details of this contribution remain unclear. We measure the proton conductivity of the AoL jelly extracted from skates and sharks. The room-temperature proton conductivity of the AoL jelly is very high at 2 ± 1 mS/cm. This conductivity is only 40-fold lower than the current state-of-the-art proton-conducting polymer Nafion, and it is the highest reported for a biological material so far. We suggest that keratan sulfate, identified previously in the AoL jelly and confirmed here, may contribute to the high proton conductivity of the AoL jelly with its sulfate groups-acid groups and proton donors. We hope that the observed high proton conductivity of the AoL jelly may contribute to future studies of the AoL function.

Keywords: Ampullae of Lorenzini; Elasmobranchii; Sharks; Skates; electrosensing cells; hydrogels; proton conductors.

Fig. 1. The AoL.

(A and B) Skates and sharks locate their prey by detecting the weak electric fields naturally generated by biomechanical activity. (C) A network of electrosensory organs called the AoL is responsible for this sense. (D) An individual ampulla consists of a surface pore connected to a set of electrosensory cells by a long jelly-filled canal. Sharks and skate can sense fields as small as 5 nV/cm despite canals traveling through up to 25 cm of noisy biological tissue. (E) A sample of the AoL jelly on an electrical device is presented. Scale bar, 0.5 mm.

Fig. 2. Proton conduction in ampullae jelly.

(A) Palladium hydride (PdH_x) protode behavior. Under an applied voltage, PdH contacts split into Pd, H⁺, and e⁻. Protons are injected into the skate jelly, whereas electrons travel through external circuitry and are measured. (B) Transient response to a 1-V applied signal in AoL jelly from R. rhina. The proton current (red) is 50 times larger than the ion current (blue). The electron current (black) is slightly smaller than the ion current. (C) Four-point probe geometry. Distinct Au contacts are used to measure voltage within the channel and to correct for any potential drop at the PdH-jelly interface. (D) Four-point probe conductivity results from R. binoculata. Conductivity increases exponentially with voltage up to about 1 V, suggesting that conduction is limited by potential barriers. Deuterium conductivity (green) at 90% D₂O humidity (RD) is half as large as proton conductivity (red) for all voltages. Ion conduction in the hydrated state (blue) is minimal. (E) TLM geometry. Varying the distance between source and drain (L_SD) distinguishes between the fixed PdH-jelly interface resistance and the varying bulk resistance. (F) R_LN as a function of L_SD for R. binoculata. A linear fit gives a bulk material proton conductivity of 1.8 ± 0.9 mS/cm.

Fig. 3. Chemical characterization of jelly.

(A) Structure of KS, which may be present in the skate (R. binoculata) AoL jelly. Proton conduction in a sulfated polymer is consistent with known conducting materials, such as Nafion or modified chitosan. (B) Compositional analysis of skate jelly from R. binoculata. The peaks denote the presence of different monomers (GalNH₂, galactosamine; GlcNH₂, glucosamine; Gal, galactose; Glc, glucose; Man, mannose; GlcA, glucuronic acid). Glucosamine and galactose, the two components of KS, are found in highest abundance. An equimolar ratio of glucosamine to galactose would be expected for KS; the slightly higher abundance of glucosamine suggests the presence of other polysaccharides in the jelly. (C) Full-scale FTIR spectrum of the skate jelly showing characteristic peaks of sulfated glycosaminoglycans (GAGs), specifically KS. a.u., arbitrary units.