Bone without minerals and its secondary mineralization in Atlantic salmon (Salmo salar): the recovery from phosphorus deficiency

Abstract

Calcium and phosphorus (P) are the main bone minerals, and P deficiency can cause hypomineralized bones (osteomalacia) and malformations. This study used a P-deficient salmon model to falsify three hypotheses. First, an extended period of dietary P deficiency does not cause pathologies other than osteomalacia. Second, secondary mineralization of non-mineralized bone is possible. Third, secondary mineralization can restore the bones' mineral composition and mechanical properties. For 7 weeks, post-smolt Atlantic salmon (Salmo salar) received diets with regular P content (RP) or with a 50% lowered P content (LP). For additional 9 weeks, RP animals continued on the regular diet (RP-RP). LP animals continued on the LP diet (LP-LP), on a regular P diet (LP-RP) or on a high P diet (LP-HP). After 16 weeks, animals in all groups maintained a non-deformed vertebral column. LP-LP animals continued bone formation albeit without mineralization. Nine weeks of RP diet largely restored the mineral content and mechanical properties of vertebral bodies. Mineralization resumed deep inside the bone and away from osteoblasts. The history of P deficiency was traceable in LP-RP and LP-HP animals as a ring of low-mineralized bone in the vertebral body endplates, but no tissue alterations occurred that foreshadow vertebral body compression or fusion. Large quantities of nonmineralized salmon bone have the capacity to re-mineralize. If 16 weeks of P deficiency as a single factor is not causal for typical vertebral body malformations, other factors remain to be identified. This example of functional bone without minerals may explain why some teleost species can afford to have an extremely low mineralized skeleton.

Zebrafish: A Resourceful Vertebrate Model to Investigate Skeletal Disorders

“…For example, ectopic mineralization was shown surrounding the eye, in the wall of the bulbus arteriosus of the heart and in the ventral skin of the dragon fish (dgf −/− ), a knock-out zebrafish model for the gene that encodes Enpp1, and modeled for generalized arterial calcification of infancy (GACI) and pseudoxanthoma elasticum (PXE) (105,106). Bone collagen in teleosts can also be deposited without being mineralized, as was shown in salmon vertebral bone (246,247) and in the dentine of replacement teeth of the African bichir (248). It is important to underline that the unmineralized collagen cannot be visualized with ARS, however, mineralization usually quickly follows collagen deposition.…”

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

“…However, this role seems less critical in teleosts than in terrestrial vertebrates since, as aquatic animals, teleosts can mobilise calcium and other elements directly from the ambient water via their gills and/or digestive system (Takagi & Yamada, ; Witten & Huysseune, ; Shahar & Dean, ). Phosphorus availability appears to be more critical than that of calcium for healthy growth in both marine and freshwater teleosts (Witten & Huysseune, ; Shahar & Dean, ), and bone does not seem to mineralise when phosphorus is absent from the diet (Witten et al , , ). Nevertheless, a specific type of bone resorption (osteocytic osteolysis) is undertaken by the osteocytes themselves and may be linked to periods of increased metabolic calcium and/or phosphorus requirement, as it occurs conspicuously in certain diadromous teleost species [e.g.…”

The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

“…However, this role seems less critical in teleosts than in terrestrial vertebrates since, as aquatic animals, teleosts can mobilise calcium and other elements directly from the ambient water via their gills and/or digestive system (Takagi & Yamada, 1992;Witten & Huysseune, 2009;Shahar & Dean, 2013). Phosphorus availability appears to be more critical than that of calcium for healthy growth in both marine and freshwater teleosts (Witten & Huysseune, 2009;Shahar & Dean, 2013), and bone does not seem to mineralise when phosphorus is absent from the diet (Witten et al, 2016(Witten et al, , 2018. Nevertheless, a specific type of bone resorption (osteocytic osteolysis) is undertaken by the osteocytes themselves and may be linked to periods of increased metabolic calcium and/or phosphorus requirement, as it occurs conspicuously in certain diadromous teleost species [e.g.…”