Biomineralization in the radula of the chiton acanthopleura granulata

Abstract

Chitons (Polyplacophora; Mollusca) are an emerging model for studies of biomineralization because they build a wide array of hardened structures from several different materials. Chitons make iron-clad teeth by coating apatite (calcium phosphate) cores with magnetite. Iron use poses a risk to animals because free iron can cause oxidative damage to tissues. We studied the process of biomineralization in the radula of the chiton Acanthopleura granulata. In this dissertation, Chapter 2 presents the first genome ever sequenced of a chiton and uses these data to examine biomineralization genes in general, as well as any changes at a genomic level due to increased iron use. We found a surprising number of previously identified biomineralization genes in chitons, even those characterized from materials that chitons do not make. Chitons have a higher number of genes directly regulated by iron than any other molluscs sequenced to date. We also describe a novel isoform of ferritin that chitons may use to protect body tissues from the iron used to mineralize their radula. Chapter 3 describes the compartmentalization across the radula that facilitates magnetite biomineralization, including an iron mineralization zone of only six tooth rows in which pH drops to ~4, and the oxidative stress that results from using free iron. Chapter 4 links chapters 2 and 3 by quantifying gene expression across the same five regions of the radula to better understand the pathways that chitons may use to regulate their physiology. We found chitons make apatite teeth using many of the same regulatory pathways used by other organisms to pattern mineralized structures. We found that chitons may protect their tissues from oxidative damage caused by iron across the radula with enzymes, but that the iron mineralization zone still damages cells. Together, this work establishes chitons as a model for the biomineralization of iron, and suggests that tooth production may be a molluscan innovation as critical as shells.