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Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes.

ABSTRACT: Cartilaginous fishes possess gel-filled tubular sensory organs called Ampullae of Lorenzini (AoL) that are used to detect electric fields. Although recent studies have identified various components of AoL gel, it has remained unclear how the molecules are structurally arranged and how their structure influences the function of the organs. Here we describe the structure of AoL gel by microscopy and small-angle X-ray scattering and infer that the material is colloidal in nature. To assess the relative function of the gel's protein constituents, we compared the microscopic structure, X-ray scattering, and proton conductivity properties of the gel before and after enzymatic digestion with a protease. We discovered that while proteins were largely responsible for conferring the viscous nature of the gel, their removal did not diminish proton conductivity. The findings lay the groundwork for more detailed studies into the specific interactions of molecules inside AoL gel at the nanoscale.

SUBMITTER: Phillips M

PROVIDER: S-EPMC8379299 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes.

Phillips Molly M Wheeler Alauna C AC Robinson Matthew J MJ Leppert Valerie V Jia Manping M Rolandi Marco M Hirst Linda S LS Amemiya Chris T CT

iScience 20210804 9

Cartilaginous fishes possess gel-filled tubular sensory organs called Ampullae of Lorenzini (AoL) that are used to detect electric fields. Although recent studies have identified various components of AoL gel, it has remained unclear how the molecules are structurally arranged and how their structure influences the function of the organs. Here we describe the structure of AoL gel by microscopy and small-angle X-ray scattering and infer that the material is colloidal in nature. To assess the rela ...[more]

PMID: 34458698

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Project description:BACKGROUND:Chondrichthyans represent a monophyletic group of crown group gnathostomes and are central to our understanding of vertebrate evolution. Like all vertebrates, cartilaginous fishes evolved concretions of material within their inner ears to aid with equilibrium and balance detection. Up to now, these materials have been identified as calcium carbonate-bearing otoconia, which are small bio-crystals consisting of an inorganic mineral and a protein, or otoconial masses (aggregations of otoconia bound by an organic matrix), being significantly different in morphology compared to the singular, polycrystalline otolith structures of bony fishes, which are solidified bio-crystals forming stony masses. Reinvestigation of the morphological and chemical properties of these chondrichthyan otoconia revises our understanding of otolith composition and has implications on the evolution of these characters in both the gnathostome crown group, and cartilaginous fishes in particular. RESULTS:Dissections of Amblyraja radiata, Potamotrygon leopoldi, and Scyliorhinus canicula revealed three pairs of singular polycrystalline otolith structures with a well-defined morphology within their inner ears, as observed in bony fishes. IR spectroscopy identified the material to be composed of carbonate/collagen-bearing apatite in all taxa. These findings contradict previous hypotheses suggesting these otoconial structures were composed of calcium carbonate in chondrichthyans. A phylogenetic mapping using 37 chondrichthyan taxa further showed that the acquisition of phosphatic otolith structures might be widespread within cartilaginous fishes. CONCLUSIONS:Differences in the size and shape of otoliths between taxa indicate a taxonomic signal within elasmobranchs. Otoliths made of carbonate/collagen-bearing apatite are reported for the first time in chondrichthyans. The intrinsic pathways to form singular, polycrystalline otoliths may represent the plesiomorphic condition for vertebrates but needs further testing. Likewise, the phosphatic composition of otoliths in early vertebrates such as cyclostomes and elasmobranchs is probably closely related to the lack of bony tissue in these groups, supporting a close relationship between skeletal tissue mineralization patterns and chemical otolith composition, underlined by physiological constraints.

Dataset Information

Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes.

Publications

Colloidal structure and proton conductivity of the gel within the electrosensory organs of cartilaginous fishes.

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