First paleoproteome study of fossil fish otoliths and the pristine preservation of the biomineral crystal host

Abstract

Otoliths are calcium carbonate components of the stato-acoustical organ responsible for hearing and maintenance of the body balance in teleost fish. During their formation, control over, e.g., morphology and carbonate polymorph is influenced by complex insoluble collagen-like protein and soluble non-collagenous protein assemblages; many of these proteins are incorporated into their aragonite crystal structure. However, in the fossil record these proteins are considered lost through diagenetic processes, hampering studies of past biomineralization mechanisms. Here we report the presence of 11 fish-specific proteins (and several isoforms) in Miocene (ca. 14.8–14.6 Ma) phycid hake otoliths. These fossil otoliths were preserved in water-impermeable clays and exhibit microscopic and crystallographic features indistinguishable from modern representatives, consistent with an exceptionally pristine state of preservation. Indeed, these fossil otoliths retain ca. 10% of the proteins sequenced from modern counterparts, including proteins specific to inner ear development, such as otolin-1-like proteins involved in the arrangement of the otoliths into the sensory epithelium and otogelin/otogelin-like proteins that are located in the acellular membranes of the inner ear in modern fish. The specificity of these proteins excludes the possibility of external contamination. Identification of a fraction of identical proteins in modern and fossil phycid hake otoliths implies a highly conserved inner ear biomineralization process through time.

Phylogenetic signal in primate tooth enamel proteins and its relevance for paleoproteomics

“…More recently, access to protein sequence data from long deceased organisms has been achieved with the aid of mass spectrometry methods (Nielsen-Marsh et al 2002; Cappellini et al 2014). Since then, the field has grown to propose a set of standards (Hendy et al 2018; Welker 2018; Hendy 2021; Warinner et al 2022), and has proven to reliably determine sequence information from samples from as much as 14.8 million years ago (Ma) (Stolarski et al 2023). The persistence of peptides for millions of years, even from temperate to warm environments, contrasts with the maximum biomolecule age of 2 Ma from ancient DNA (aDNA) under permafrost conditions, which are considered ideal conditions (Kjær et al 2022).…”